Covariation of Learning and "Reasoning" Abilities in Mice: Evolutionary Conservation of The Operations of Intelligence

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Covariation of Learning and "Reasoning" Abilities in Mice: Evolutionary

Conservation of the Operations of Intelligence
Article in Journal of Experimental Psychology Animal Behavior Processes · March 2012

DOI: 10.1037/a0027355 · Source: PubMed
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Journal of Experimental Psychology: © 2012 American Psychological Association

Animal Behavior Processes 0097-7403/12/$12.00 DOI: 10.1037/a0027355
2012, Vol. , No. , 000 – 000
Covariation of Learning and “Reasoning” Abilities in Mice: Evolutionary

Conservation of the Operations of Intelligence
Christopher Wass, Alexander Denman-Brice, Chris Rios, Kenneth R. Light, Stefan Kolata, Andrew M. Smith,
and Louis D. Matzel
AQ: 1 Rutgers University
Contemporary descriptions of human intelligence hold that this trait influences a broad range of cognitive
abilities, including learning, attention, and reasoning. Like humans, individual genetically heterogeneous
mice express a “general” cognitive trait that influences performance across a diverse array of learning and
attentional tasks, and it has been suggested that this trait is qualitatively and structurally analogous to
general intelligence in humans. However, the hallmark of human intelligence is the ability to use various
forms of “reasoning” to support solutions to novel problems. Here, we find that genetically heteroge-
neous mice are capable of solving problems that are nominally indicative of inductive and deductive
forms of reasoning, and that individuals’ capacity for reasoning covaries with more general learning
abilities. Mice were characterized for their general learning ability as determined by their aggregate
performance (derived from principal component analysis) across a battery of five diverse learning tasks.
These animals were then assessed on prototypic tests indicative of deductive reasoning (inferring the
meaning of a novel item by exclusion, i.e., “fast mapping”) and inductive reasoning (execution of an
efficient search strategy in a binary decision tree). The animals exhibited systematic abilities on each of
these nominal reasoning tasks that were predicted by their aggregate performance on the battery of
learning tasks. These results suggest that the coregulation of reasoning and general learning performance
in genetically heterogeneous mice form a core cognitive trait that is analogous to human intelligence.
AQ: 2 Keywords: intelligence, learning, reasoning, working memory, fast mapping, phylogenetics
Studies of individual differences in mental abilities in nonhu- (December 13, 1994) signed by 52 intelligence researchers, it was AQ: 3
man animals have increased dramatically during the past decade, asserted that intelligence was “a very general mental capability
and this work has served as an impetus to further delineate the that, among other things, involves the ability to reason, plan, solve
behavioral processes and neural mechanisms that underlie general problems, think abstractly, comprehend complex ideas, learn
intelligence. Over a century ago, Spearman described “general quickly and learn from experience.” A committee of the American
intelligence” (i.e., “g”), noting that a single factor could account Psychological Association (1995) stated that “Individuals differ AQ: 4
for a large portion of the underlying variance in performance from one another in their ability to understand complex ideas, to
across diverse cognitive tasks. Spearman (1904) concluded that adapt effectively to the environment, to learn from experience, and
regardless of the specific demands of a task, performance on that to engage in various forms of reasoning to overcome obstacles.
task is determined by both domain-specific abilities (e.g., spatial Concepts of “intelligence” are attempts to clarify and organize this
ability) as well as by g (i.e., general intelligence). It is the recog- complex set of phenomena.” While there is an apparent consensus
nition of this latent influence on the execution of most cognitive regarding the functional consequences of intelligent behavior,
tasks that underlies the rationale for contemporary tests of human
these “definitions” are simultaneously nebulous in content and
intelligence.
expansive in scope.
Despite decades of often vigorous debate, a single, a widely
While a widely accepted definition of “intelligence” has not
accepted definition of “intelligence” has yet to be agreed upon.
fully materialized, most descriptions (including those provided
Nevertheless, consensus has emerged regarding the operations
above) state that intelligent behavior involves the ability to “adapt
impacted by intelligence. In an article in the Wall Street Journal
to the environment” and to “learn quickly.” These characteristics,
like colloquial impressions of intelligence, suggest that learning is
a critical component of, if not critically influenced by, intelligence.
For instance, rates of learning among humans are often predicted
Christopher Wass, Alexander Denman-Brice, Chris Rios, Kenneth R. by psychometric tests of IQ (for reviews, see Gettinger, 1984;
Light, Stefan Kolata, Andrew M. Smith, and Louis D. Matzel, Department Jensen, 1989). In fact, Jensen has concluded that general learning
of Psychology, Rutgers University.
factors (extracted from performance across large numbers of
This work was supported by a grant from the U.S. Public Health Service
(National Institute of Aging, AG022698) to L.D.M.
learning tasks) are so highly related to the general intelligence
Correspondence concerning this article should be addressed to Louis D. factor extracted from psychometric tests that “learning and psy-
Matzel, Program in Behavioral Neuroscience, Department of Psychology, chometric abilities (general intelligence) are essentially one and
Rutgers University, Piscataway, NJ 08854. E-mail: [email protected] the same” (Jensen, 1998). It is notable that occasional reports of a
1
2 WASS ET AL.
lack of correlation between performance on single learning tasks Logical inference, as exemplified here, is often described as a
and measures of general intelligence may at times be attributable hallmark of reasoning.
to the high task-specific variability inherent to measures of per- Although fast mapping has been extensively studied in humans,
formance on a single task, such that the influence of a general there have been few attempts (except in two dogs and one chim-
factor on that task is relatively small (and thus, not detected by a panzee) to assess whether nonhuman animals are capable of this
probability test). Furthermore, on elemental tasks that all subjects cognitive process. Briefly, Kaminski, Call, and Fischer (2004),
can presumably master, any correlation between learning and demonstrated that a Border Collie (also see Pilley & Reid, 2011)
general intelligence is dependent on the measurement of learning was able (on first command) to retrieve a novel object (identified
rate or speed of responding, a requirement that has at times been by a novel term) from among set of over 200 previously learned
overlooked (see Jensen, 1998, p. 275 for discussion relevant to objects. Kaminski et al. concluded that the Border Collie was able
AQ: 5 human learning, and Kolata, 2008, for a discussion relevant to the to correctly retrieve the novel object through the use of inferential
present utilization of measures of learning performance; for alter- exclusion principles, that is, the novel word used in the voice
native data and interpretation, see Williams & Pearlberg, 2006). command was inferred to mean to retrieve the novel object.
While the capacity for learning is indicative of intelligence, Hashiya and Kojima (2001) demonstrated that a chimpanzee was
definitions of intelligence (such as those provided above) make also able to use inferential exclusion in order to correctly match a
reference to myriad processes beyond learning. Along with the novel voice to a novel portrait when two previously learned
ability to learn, most definitions of this trait make primary refer- portraits (distracters) were present. Based on the limited observa-
ences to an individual’s capacity to “think rationally,” “reason,” tions of fast mapping in nonhuman animals, it is reasonable to ask
“engage in reasoning,” or colloquially, “to figure out novel solu- whether mice are capable of utilizing similar basic reasoning, and
tions” based on limited experience. Thus, the efficacy of reasoning whether the fast mapping abilities of mice covary with the general
is widely considered to be a critical component of intelligence learning abilities of these animals.
(Manktelow, 1999), and most intelligence test batteries include Prior studies have demonstrated the existence of a general
components specifically intended to characterize an individual’s cognitive factor in genetically heterogeneous mice, and this latent
capacity for reasoning. In fact, many modern tests of intelligence influence on diverse learning abilities is in many ways analogous
(e.g., the Raven’s Progressive Matrix) are weighted almost exclu- to general intelligence in humans. Specifically, we have shown
sively toward this ability. that when genetically heterogeneous mice are assessed on batteries
While it has been empirically determined that human intelli- of as many as nine diverse learning tasks, as much as 28 –50% of
gence (including its expression on tests of reasoning) and learning the variance in performance across these tasks can be accounted
abilities covary (Gettinger, 1984; Jensen, 1989), there have been for by a single factor (Kolata et al., 2008; Kolata et al., 2010;
no attempts to assess the relationship between general learning Light, Kolata, Denman-Brice, Zagalsky, & Matzel, 2008; Matzel
abilities and reasoning in nonhuman animals. In this regard, it was et al., 2003; Matzel et al., 2006; Matzel, Grossman, Light,
until recently a common assertion that reasoning was beyond the Townsend, & Kolata, 2008; also, see Galsworthy, Paya-Cano,
capacity of nonhuman animals. In contrast to this assertion, dem- Monleón, & Plomin, 2002; Locurto, Fortin, & Sullivan, 2003).
onstrations of behaviors that are nominally indicative of reasoning Moreover, it has been determined that the efficacy of processing
in nonhuman animals have begun to be reported. Briefly, species components of working memory (i.e., capacity and selective at-
such as monkeys (McGonigle & Chalmers, 1977; Rapp, Kansky, tention) covary with an animal’s general learning ability (Kolata et
& Eichenbaum, 1996), chimpanzees (Boysen, Berntson, Shreyer, al., 2005, 2007), and furthermore, working memory training reg-
& Quigley, 1993), rats (Dusek & Eichenbaum, 1997; Roberts & imens promote an increase in animals’ general learning abilities
AQ: 6 Phelps, 1994), and pigeons (Wynne, 1997; Lazareva, 2006 1853) (Light et al., 2010; Matzel et al., 2011). These observations cor-
have all demonstrated the capacity for transitive inference, an respond with studies of humans which have indicated that working
ability that, at least in some instances, has been asserted to depend memory capacity covaries with an individual’s general intelligence
on deductive forms of reasoning (for alternative explanations, see (Conway, Kane, & Engle, 2003; Engle, Laughlin, Tuholski, &
General Discussion & Shettleworth, 2010). Another task (that we Conway, 1999; Jaeggi et al., 2009). Thus, the processes that AQ: 7
will adapt here for the assessment of mice) that has been used to regulate the general learning abilities of mice are to some degree
assess reasoning abilities in nonhuman animals is “fast mapping.” homologous with those implicated in establishing general intelli-
Fast mapping is a mental process whereby a new concept can be gence in humans.
learned based on a logical inference derived from a single expo- As reasoning abilities are widely considered to epitomize the
sure to limited information. Fast mapping (Care & Bartlett, 1978) functional operations of “intelligence” (and comprise a core com-
is believed to play a critical role in the extraordinarily rapid and ponent of all definitions of intelligence), the work reported in the
seemingly effortless acquisition of information during early human present article was aimed to determine whether laboratory mice are
development, and explains (in part) the prodigious rate at which capable of behaviors that are analogous to behaviors described as
children gain vocabulary. For example, when faced with a group of “reasoning” among humans, and if so, whether the animals’ ca-
familiar items described by familiar words, an individual will pacity for this reasoning-like behavior covaries with their general
quickly associate an unfamiliar word with a novel item added to learning abilities. To assess the hypothesis that general learning
the otherwise familiar set (“inference by exclusion”), and this abilities and reasoning-like cognitive performance covary in lab-
association requires no overt “pairing” of the novel word and its oratory mice, we first utilized a fast mapping-based task which is
corresponding novel item. Over time, the word’s approximate commonly asserted to reflect a subject’s capacity for deductive
meaning becomes more refined as it is seen in other contexts. reasoning (e.g., Carey & Bartlett, 1978).
REASONING AND GENERAL LEARNING 3
Experiment 1A familiarize them with the novel reinforcer. On the acclimation day,
each mouse was placed in the four alleys of the maze, but the
In order to assess whether an animal’s general learning and openings between the alleys were blocked (with black Plexiglas)
deductive reasoning abilities were jointly regulated, we first char- so that the animals could not navigate between them. Each animal
acterized the general learning ability of individual animals in a was confined to the start and subsequent two alleys for 4 min, and
five-task learning battery that has been previously described (e.g., for 6 min in the last (goal) alley, where three food pellets were
Matzel et al., 2003, 2006). A principal component analysis was present in the food cup. This acclimation period promotes stable
then applied to animals’ performance on these five learning tasks and high levels of activity on the subsequent training day. On the
in order to derive each animal’s factor score (a measure of each training day, each animal was placed in the start box and allowed
animal’s aggregate performance across all learning tasks; see be- to traverse the maze until it reached the goal box and consumed the
low). Having ascertained the general learning ability of each single food pellet present in the cup. Upon consuming the food, the
animal, we then assessed the same animals on a fast-mapping task. animal was returned to its home cage for a 20 min intertrial
Animals’ general learning performance was then compared to their interval (intertribal interval, ITI), during which the apparatus was
performance on the fast mapping task so as to determine the degree cleaned. After the ITI, the mouse was returned to the start box to
of covariance between individuals’ capacity for deductive reason- begin the next trial, and the sequence was repeated for five trials.
ing and general learning abilities.
Both the latency and errors (i.e., a turn in an incorrect direction,
including those which result in path retracing) to enter the goal box
Method were recorded on each trial.
Spatial water maze. Animals were immersed in a round pool
Subjects. A sample of 47 genetically heterogeneous male of opaque water from which they were able to escape onto a
CD-1 mice were obtained from Harlan Laboratories (Indianapolis, hidden (i.e., submerged) platform. The latency for animals to find
IN) at 45 days of age. Owing to an experimenter error during fast the platform decreased across successive trials. In this task, per-
mapping training, six animals could not be tested in this task. Upon formance of animals can improve across trials despite the animals
arrival in our vivarium, animals were individually housed in stan- beginning each trial from a new start location. Such a procedure
dard shoe box cages and were allowed ad libitum access to food
mitigates egocentric navigation and promotes the animals’ depen-
and water. All animals were allowed to acclimate to the vivarium,
dence on extramaze spatial landmarks. Typically, rodents‘ perfor-
which was maintained on a 12 hour light/dark cycle, for a period
mance in the water maze does not rely on fixed motor patterns (i.e.,
of two weeks. During this period, the animals were handled by the
performance improves despite the animal’s irregular starting loca-
experimenter for 90 sec/day in order to mitigate differential stress
tion) or the presence of discernable cues within the maze (e.g.,
responses to the experimenter.
visual, tactile, or olfactory signals). Instead, performance is depen-
Learning battery. To quantify animals’ general learning
dent on the stability of extramaze cues, or “landmarks,” and is said
abilities, we evaluated animals’ performance on a battery of five
to reflect the animals’ representation of its environment as a
diverse tasks that impinged on different domains of learning,
“cognitive map.”
sensory/motor, and motivational systems. All of the animals were
We employ a protocol in which mice exhibit significant reduc-
tested on these five tasks in the following order: Lashley III Maze,
spatial water maze, passive avoidance, associative fear condition- tions in their latency to locate the escape platform within 5–10
ing, and odor guided discrimination. Two days of rest intervened training trials. To support rapid acquisition, animals were confined
between each successive task in the learning battery. For tasks in a clear Plexiglas cylinder on the safe platform for 6 min on the
utilizing food reinforcers, animals were food deprived 48 hours day prior to training. Second, a considerably longer ITI (10 min)
prior to training by allowing only 90 min access to food within 2 was used than is typical (cf., 90 sec). Lastly, the maze, surround,
hours of the end of the light cycle. and water were black and visual cues were constructed of patterns
Lashley III maze. The Lashley III maze consisted of a start of lights.
box, four interconnected alleys, and a goal box containing a food A round black pool (140 cm diameter, 56 cm deep) was filled to
reward. (For an illustration of the Maze, see Matzel et al., 2003.) within 24 cm of the top with water made opaque by the addition of
Efficient performance in the maze required that the animal make nontoxic, water soluble, black paint. A hidden 11 cm diameter
five spatial alternations to reach the goal box. Over trials, the black platform was in a fixed location 1.5 cm below the surface of
errors (i.e., wrong turns or retracing) committed in the animal’s the water midway between the center and perimeter of the pool.
approach to the goal box decreased. The maze (scaled for mice) The pool was enclosed in a ceiling-high black curtain on which
was constructed of black Plexiglas. Each alley measured 58 ⫻ 6 five different shapes (landmark cues) were variously positioned at
cm, and had 16 cm high walls. A goal box was (20 cm long) was heights (relative to water surface) ranging from 24 –150 cm. Four
located 10 cm from the end of the last alley. A 2 cm diameter white of these shapes were constructed of strings of white LEDs (spaced
cup was located in the rear portion of the goal box, and 45 mg at 2.5 cm intervals) and included an “X” (66 cm arms crossing at
BioServe (rodent grain) pellets served as reinforcers. Illumination angles 40o from the pool surface), a vertical “spiral” (80 cm long,
was 80 Lux at the floor of the maze. The maze was isolated behind 7 cm diameter, 11 cm revolutions), a vertical line (31 cm) and a
a shield of white Plexiglas to prevent the use of extramaze land- horizontal line (31 cm). The fifth cue was constructed of two
mark cues. adjacent 7 W light bulbs (each 4 cm diameter). A video camera
Food-deprived animals were acclimated and trained on two was mounted 180 cm above the center of the water surface. These
successive days. On the day prior to acclimation, all animals were cues provided the only illumination of the maze, totaling 172 Lux
provided with three BioServe food pellets in their home cages to at the water surface.
4 WASS ET AL.
On the day prior to training, each animal was confined to the compound aversive stimulus comprised of a bright (550 Lux)
escape platform for 360 sec. white light and “siren” (58 dBc above the 50 dB background,
Training was conducted on the two subsequent days. On Day 1 2.4 –3.7 kHz; Radio Shack sound oscillator, Model 273– 057) was
of training, animals were started from one of three unique locations initiated.
on each of six trials. (The pool was conceptually divided into four Animals were placed on the platform behind the closed exit
quadrants, and one starting point was located in each of the three door. After 4 min of confinement, the door was retracted and the
quadrants that did not contain the escape platform. The starting latency of the animal to leave the platform and make contact with
point on each trial alternated between the three available quad- the grid floor was recorded. Prior to training, step-down latencies
rants.) An animal was judged to have escaped from the water (i.e., typically range from 8 –20 sec. Upon contact with the floor, the
located the platform) at the moment at which four paws were aversive stimulus (light, noise, and vibration) was presented for 3
situated on the platform, provided that the animal remained on the sec. Upon initiation of the aversive stimulus, mice retract onto the
platform for at least 5 sec. Each animal was left on the platform for safe chamber, at which time the platform door was closed and they
a total of 20 sec, after which the trial was terminated. Trials were were again confined for 4 min. At the end of this interval, the door
spaced at 10 min intervals, during which time the animals were was opened and the latency of the animal to exit the platform and
held in their home cages. On each trial, a 90 sec limit on swimming step onto the grid floor (with no aversive stimulation) was again
was imposed, at which time any animal that had not located the recorded. The ratio of posttraining to pretraining step-down laten-
escape platform was placed by the experimenter onto the platform, cies was calculated for each animal and served to index learning.
where it remained for 20 sec. It has previously been determined that asymptotic performance is
Animals were observed from a remote (outside of the pool’s apparent in group averages following 2–3 training trials; thus,
enclosure) video monitor, and animals’ performance was recorded performance after a single trial reflects, in most instances, subas-
on video tape for subsequent analysis. Day 2 of training proceeded ymptotic learning.
as did Day 1, albeit with only four trials. After the last training Associative fear conditioning. In this task the animals re-
trial, a 90 min retention period began, after which animals were ceived a tone (conditional stimulus, CS) paired with a mild foot-
tested with a “probe” trial. On the probe test, the escape platform shock (US). Two distinct experimental chambers were used (a AQ: 8
was removed from the pool, and all animals were started from training context and a novel context). Each box was contained
the first position for that day. A 90 sec test was conducted in within a sound and light-attenuating chamber. The training box
which the animals’ time searching in the target quadrant (where (16.5 ⫻ 26.5 ⫻ 20 cm) was brightly lit (50 Lux) with a clear
the escape platform was previously located) and nontarget Plexiglas front/back, and one stainless steel and one clear Plexiglas
quadrants were recorded. side wall. The floor was composed of a steel grid (5 mm spacing)
One-trial passive avoidance. Animals learn to suppress from which a 0.6 mA constant current footshock could be deliv-
movement to avoid contact with aversive stimuli. This “passive ered from a shock scrambler (Lafayette Instruments, Lafayette,
avoidance” response is exemplified in step-down avoidance pro- IN). The novel chamber (23 ⫻ 21.5 ⫻ 19 cm) was dimly lit (4
cedures, where an animal is placed on a platform, whereupon Lux) and all of the walls and the floor were composed of clear
stepping off of the platform it encounters a footshock. Following Plexiglas. In both boxes the tone (60 dB, 2.9 kHz) was delivered
just a single encounter with shock, animals are subsequently re- by a piezoelectric buzzer (Med Associates, EV-203a).
luctant to step off of the safe platform. The animals’ reluctance to The animals were acclimated to the training and novel contexts
leave the platform is believed to not reflect fear, because typical by placing each animal in both boxes for 20 min on the day before
fear responses are not expressed in animals engaged in the avoid- training. Training on the subsequent day occurred in a single 18
ance response. Upon stepping off the platform, animals here were min session during which the animals received three tone-shock
exposed to a compound of bright light and loud oscillating noise pairings after 4 min, 10 min, and 16 min. The CS presentation
rather than shock, so as not to duplicate stimuli between tasks (see consisted of a pulsed (0.7 sec on, 0.3 sec off) 20 sec tone.
fear conditioning, below). Like more common procedures, our Coincident with the offset of the tone, shock (US) was presented AQ: 9
variant of this task supports learning after only a single trial (i.e., for 500 msec. The following day the animals were placed in the
subsequent step-down latencies are markedly increased). novel chamber where they received the same presentation of tones
A chamber illuminated by dim (50 Lux) red light was used for but without the shock. (As it was critical to measure performance
training and testing. Animals were confined to circular (“safe”) during acquisition, tests of the tone in the novel chamber are not
chamber (10 cm diameter, 8 cm high). The walls and floor of this reported here. This test was conducted simply to maintain compa-
chamber were white, and the ceiling was translucent orange. The rability to previous work in our laboratory.)
floor was comprised of plastic rods (2 mm diameter) arranged to To quantify conditioned fear responses, the animal’s behavior
form a pattern of 1 cm square grids. A clear exit door (3 CM was videotaped and both the time spent freezing 20 sec prior to the
square) was flush with the floor of the safe compartment, and the initiation of the tone as well as freezing during the tone was
door was able to slide horizontally to open or close the compart- determined. Freezing was defined as period of 1 sec or greater
ment. The bottom of the exit door was located 4 cm above the floor when all of the animal’s paws remained anchored in-place to the
of a second circular chamber (20 cm diameter, 12 cm high). This grid floor and the animal’s ears were retracted. Freezing responses
“unsafe” chamber had a clear ceiling and a floor comprised of 4 were scored by an observer who was unaware of the animal’s
mm wide aluminum planks that formed a pattern of 1.5 cm square performance on other behavioral tests. Conditioned responses to
grids oriented at a 45o angle relative to the grids in the safe the CS were defined as freezing during the tone presentation minus
compartment. When an animal stepped from the safe compartment freezing prior to the tone. For purpose of ranking the animals, CS
through the exit door onto the floor of the unsafe compartment, a freezing during the second training trial was used.
Odor guided discrimination. Rodents rapidly learn to use tered on the final (critical) test trial. (This procedure would be
odors to guide appetitively reinforced behaviors. Here, mice repeated on the day prior to the critical test.)
learned to navigate a square field in which unique odor-marked On Day 2 of training, animals were acclimated to the training
(e.g., almond, lemon, mint) food cups were located in three cor- apparatus which was constructed of black Plexiglas. The training
ners. Although food was present in each cup, it was only accessible apparatus consisted of a start box measuring 20 ⫻ 14 ⫻ 20 cm and
to the animals in the cup marked by mint odor. An animal was a field portion. The walls (46 cm in length and 20 cm high) of the
placed in the empty corner of the field, after which it explored the field portion radiated from the start box at an approximate 145
field and eventually retrieved the single piece of available food. On degree angle and were connected to the back wall of the field
subsequent trials, the location of the food cups was changed, but which was measured 60 cm in length and 20 cm high. Located
the accessible food was consistently marked by the same odor, within the start box was a square block of black Plexiglas mea-
mint. On successive trials, animals required less time to retrieve suring 7.5 ⫻ 7.5 ⫻ 1.5 cm which was fastened to the base of the
the food and made fewer search errors (see below) directed at food apparatus by Velcro. In the center of the block was a food port
cups in which food was not available. With this procedure, near measuring 1.5 cm in diameter and 1 cm in depth. This served as the
errorless performance is typically observed within 3– 4 training reinforcer (45 mg BioServ dustless precision pellets) location.
trials. Three identical blocks were also placed in the field portion of the
A black Plexiglas 60 cm square field with 30 cm high walls was apparatus. An inaccessible food port (to which a food reinforcer
located in a dimly lit (10 fc) testing room with a high ventilation was loaded in all cups) measuring 1 cm in diameter was drilled
rate (3 min volume exchange). Three 4 ⫻ 4 ⫻ 2.0 cm (l, w, h) into the side of each food cup. A 2 mm hole was drilled directly
aluminum food cups were placed in three corners of the field. A into the center of the inaccessible food port until it protruded into
food reinforcer (30 mg portions of chocolate flavored puffed rice) the accessible food port. Food placed in the port served as an odor
was placed in a 1.6 cm deep, 1 cm diameter depression in the stimulus to ensure that the smell of food in the target cup could not
center of each cup. The food in two of the cups was covered (1.0 differentially guide the animal’s behavior during training or test-
cm below the surface of the cup) with a wire mesh so that it was ing. During this acclimation phase all of the possible food loca-
not accessible to the animal, while in the third cup (the “target” tions (a total of four locations) were baited. Initially the animals
were confined to the start box for a period of five minutes. After
cup), the food could be retrieved and consumed. A cotton-tipped
this time period had elapsed the clear Plexiglas door (separating
laboratory swab, located between the center and rear corner of
the start box from the field) was removed allowing the animal to
each cup, extended vertically 3 cm from the cups’ surface.
venture into the field portion of the apparatus where it was con-
Immediately prior to each trial, fresh swabs were loaded with 25
fined for another period of 5 min.
␮l of either lemon, almond, or mint odorants (McCormick flavor
On Day 3, the training process was begun. The animals were
extracts). The mint odor was always associated with the target food
trained in two distinct phases. During the first phase, animals were
cup. It should be noted that, in pilot studies, the odor associated
placed in the start location with a sample object (chosen from the
with food was counterbalanced across animals, and no discernible
eight figures that the animals were exposed to on Day 1) that had
differences in performance were detected in response to the dif-
a reinforcer located in a recessed cup beneath it. Once the animal
ferent odors. On the test day, animals received four training trials
retrieved the reinforcer, the door was opened and the animal was
in the field with three food cups present. On each trial, an animal allowed to venture into the field portion where only the sample
was placed in the empty corner of the field. On Trial 1, the object’s paired associate (target object) was located. Under this
reinforcing food was available to the animal in the cup marked by target object was a second reinforcer. Training using this same
mint odor. The trial continued until the animal retrieved and procedure was continued (with a 6 min intertrial interval) for the
consumed the food from the target cup, after which the animal was two additional paired associates. This procedure was repeated for
left in the chamber for an additional 20 sec and then returned to its 4 days (a total of eight exposures to each of the three stimulus
home cage to begin a 6 min ITI. On Trials 2– 4, the location of the pairs), with the order of exposure to each pair randomly deter-
food cups was rearranged, but the baited cup was consistently mined on each day. After paired associate training (Phase 1) was
marked by the mint odor. Both the corner location of the mint odor complete, Phase 2 of training began on the subsequent day, at
and its position relative to the remaining odors were changed on which time animals were exposed to an object from one pair (the
each trial. On each trial, the errors committed by the mouse were sample) and were allowed to collect food from under its paired
recorded. An error was recorded any time an animal made contact associate (the target). However, on these trials the target object
with an incorrect cup, or its nose crossed a plane parallel to the was placed in a field containing two distracter objects (objects that
perimeter of an incorrect cup. had previously been paired with a different sample object). Six
Fast mapping procedure. Two weeks after the completion such training trials were conducted per day such that each pair of
of the previous test, animals’ capacity for deductive reasoning was objects was encountered two times each day. This phase of training
determined based on their performance in a fast mapping task spanned 8 days (a total of 16 additional exposures to each stimulus
F1 (illustrated in Figure 1). On the first day of training, animals were pair), at the end of which all animals performed near errorlessly,
placed in a square open field constructed of white Plexiglas (46 ⫻ choosing the correct target on at least five of the last six trials.
46 ⫻ 13 cm) for 15 min. Located within the field were eight One day after the completion of Phase 2 paired-associate train-
uniformly distributed objects (small plastic figurines, Mattel Corp., ing, the animals were again placed in the open field (as described
01-09TL) that would later be used to form paired associates. This above) with the six paired-associate objects and two novel objects
initial exposure was intended to familiarize animals to these ob- (previously encountered only in the open field) uniformly distrib-
jects, as two of the eight objects would otherwise only be encoun- uted throughout the field. Again, this was intended to moderate
6 WASS ET AL.
Figure 1. An illustration of the procedure for the “fast mapping” task. During Phase 1, animals were taught
to associate pairs of objects (“paired associates). In Phase 2, animals were allowed to find the relevant paired
associate within a field that contained several objects, all of which had previously undergone paired associate
training. In Phase 3, a “fast mapping” test was administered. On this test trial, animals were exposed to a novel
sample object, and then allowed to explore the test field which contained a set of familiar objects (ones that had
an established meaning based on prior paired-associate training) and one novel object. (Note: For simplicity, the
directional arrows illustrated above all point to a correct target object located in the center position of the test
field. During actual trials, the location of the correct target was randomly determined).
any differential responding to the two novel objects that animals the underlying influence across all tasks was domain-independent
would encounter on the critical fast mapping test trial. On the (i.e., “general”).
subsequent day, animals received a single test trial to assess their The performance of individual animals across all learning tasks
capacity for fast mapping. A fast mapping test trial consisted of was first analyzed with a principal component analysis. This is a
exposure to a novel (previously unencountered) sample object and variable reduction procedure that uses an orthogonal transforma-
a novel target object placed within a field of three objects, two of tion to convert a set of independent observations (potentially
which were previous paired associates (i.e., which had acquired correlated variables) into a set of uncorrelated variables (i.e.,
specific meaning). After exposure to the novel sample and retrieval principal components). The goal of this analysis is to provide a
of the reinforcer located beneath it, the animals were allowed to reasonable characterization of the complete data set by reducing a
explore the field of three objects (two previously trained on one correlation matrix to the fewest number of factors that can describe
novel to the test context). Target choices were then recorded until the pattern of correlations. The principal factor is that factor which
the piece of food located under the novel object was collected. can explain the largest amount of variance. Previous work has
indicated that as much as 28 – 48% of the variance in performance
Results and Discussion across the five learning tasks reported here can be accounted for by
Here, we assessed 41 genetically heterogeneous CD-1 mice on a single factor (see Kolata et al., 2008, for a complete description).
a battery of five learning tasks (i.e., Lashley III maze, passive In the present study, a principle component factor analysis of
avoidance, odor guided discrimination, Morris water maze, and animals’ performance on the five learning tasks (see Table 1) T1
associative fear conditioning) designed to tax different sensory/ indicated that performance on all tasks were influenced by a single
motor, and information processing systems. These tasks placed source of variance. That factor (eigenvalue of 1.72) accounted for
unique sensory, motor, motivational, and information processing 29% of the variance in the performance across all of the learning
demands on the animals, thereby maximizing the likelihood that tasks. From that analysis, a general learning factor score was
Table 1 revealed a significant difference between the best and the worst
Factor Loadings From The Principal Components Analysis learners, p ⬍ .002. No other comparison was significant, although
(n ⫽ 41) For Animals’ Performance On The Five Learning a trend toward a difference was observed when the intermediate
Tasks In Experiment 1A learners were compared to the animals of low learning abilities,
p ⬍ .09.
General learning factor It is important to note that across the entire sample of 41
Lashley III Maze ⫺.60 animals, 22 animals made no fast mapping errors, and on average,
Fear Conditioning ⫺.52 animals made only .4 errors. This number of errors is far below
Passive Avoidance ⫺.72 that which would occur by chance (where one [or potentially more
Odor Discrimination ⫺.61 if errors were repeated] errors would be expected in a random
Morris Water Maze ⫺.40
search), ␹2(41, 2) ⫽ 22.87, p ⬍ .0001, indicating that rodents are
eigenvalue 1.72
% variance .29 indeed capable of nominal deductive reasoning as represented by
performance on a fast-mapping task.
One might interpret the results of this experiment as the conse-
quence of the animals simply approaching the novel object in the
calculated for each of the animals. A factor score is analogous to field rather than deducing that the novel target object was the
an average z score of an animal’s performance on the five learning correct choice in response to the novel sample object. However, it
tasks, with each score weighted according to the individual tasks should be reiterated that prior to and again at the completion of
loading on the primary (general learning) factor. Thus, an animal’s paired-associate training, animals were exposed equally to all
factor score is a quantification of that animal’s position in the sample and test objects to mitigate this potential influence. Nev-
distribution of general learning abilities. ertheless, the “novel” test object was designated as novel based on
In subsequent analyses, animals would be compared based on its having undergone no prior paired associate training, and as
their aggregate performance across all learning tasks. This was such, was less familiar to the animals than were the two distractor
accomplished by separating animals into groups comprised of objects (that had undergone previous paired associate training). A
high, intermediate, and low factor scores (based on the principal more complete test of the possibility that the relative novelty of the
components analysis presented above). That is, the factor scores test object, as opposed to fast mapping, could account for the
(of each individual) were ranked, and the top, middle, and bottom results presented here is provided in Experiment 1B.
thirds of these ranked scores were used to construct groups of
animals representing high, intermediate, and low general learning Experiment 1B
F2 abilities. Figure 2 presents the learning performance on each
learning task of animals characterized as having high or low With a task that was procedurally and conceptually analogous to
general learning abilities. As is evident from this figure, animals so fast mapping, in Experiment 1A, we ostensibly demonstrated that
classified are clearly distinguishable, not only according to their mice were capable of making choices based on inferential exclu-
aggregate performance, but also on individual learning tasks. sion. Furthermore, performance on the fast-mapping task was
After completion of the learning battery, animals began training significantly correlated with animals’ aggregate performance in
on a task intended to assess fast mapping. Animals were first battery of learning tests, suggesting that nominal reasoning and
required to learn associations between three pairs of objects (small general learning abilities were jointly regulated. However, on the
plastic figurines) in order to obtain a food reward, and their critical fast mapping test trial, a correct choice was indicated by an
capacity for fast mapping was then evaluated. A fast mapping test animal approaching a test stimulus (in response to a novel sample)
trial consisted of exposure to a novel (previously untrained) sam- that was less familiar than the comparison objects (that had un-
ple object and a novel (previously untrained) target object that was dergone paired-associate training). A correct choice was presumed
located in a field of three objects (where the remaining two objects to reflect the animal’s decision that in a field of familiar objects,
were previously paired associates). Target choices were then re- the novel sample must be associated with the more novel test
corded until the reinforcer located beneath the novel object was object. In that task, animals had been preexposed (in a nontest
collected. If animals were employing inferential exclusion, they environment) to all stimuli so as to reduce the nominal novelty of
should make the inference that since the sample object located in the sample and test stimuli at the time of test. Nevertheless, at the
the start box was novel, they should direct their choice toward the time of the critical test, the novel test stimulus was less familiar to
novel object in the test field. The number of errors (incorrect target the animals than were the previously trained stimuli, raising the
choices) that the animals made was recorded and compared to their possibility that animals were simply attracted to the more novel
factor scores (their aggregate performance in the learning battery, stimulus, rather than selecting that object through the process of
where lower scores ⫽ higher aggregate learning performance) inferential exclusion. Given that the animals were food deprived
which revealed a significant correlation, r(39) ⫽ .44, p ⬍ .01, and the familiar objects in the test field were previously paired
indicating that animals with higher aggregate learning abilities also with food, this seemed an unlikely explanation for the animals’
made fewer fast mapping errors. This correlation was reflected in performance. Nevertheless, based on the procedure in Experiment
marked differences in performance across animals of high, inter- 1A, this possibility cannot be excluded.
F3 mediate, and low general learning abilities (see Figure 3). A In order to ascertain whether the subjects’ performance on the
comparison of the fast mapping errors of these three groups using fast mapping test in Experiment 1A was influenced by a propensity
a one way ANOVA revealed a main effect of group (i.e., learning for novelty seeking, in Experiment 1B we implemented a relevant
ability), F(2, 38) ⫽ 5.53, p ⫽ .008. An LSD post hoc analysis control procedure into the fast mapping task. Using a group of
8 WASS ET AL.
A: Lashley III Maze B: Odor-Guided Discrimination

30
18
Errors to Locate Reinforcer
Errors to Locate Reinforcer

High Aggregate Learning Abilities 16 High Aggregate Learning Abilities
25
Low Aggregate Learning Abilities 14
Low Aggregate Learning Abilities
20 12
10
15 8
6
10
4
2
5
0
1 2 3 4 5 1 2 3 4
Trials Trials
C: Morris Water Maze D: Fear Conditioning

Latency (sec) to Locate Platform
80 High Aggregate Learning Abilities High Aggregate Learning Abilities

Low Aggregate Learning Abilities Low Aggregate Learning Abilities
Freezing During CS (Sec)

70 12
60
10
50
8
40
30
6
20
4
10
1 2 3 4 5 6 7 8 9 10 1 2 3
Trials Trials
E: Passive Avoidance
Post/Pre-Step Down Latency
LOW HIGH
Aggregate Learning Abilities
Figure 2. Performance on individual tasks of animals of highest and lowest general cognitive abilities. General
learning abilities were determined by factor scores (of individual animals) derived from a principal component
analysis of the acquisition data from all five learning tasks. Illustrated is the mean performance of animals of
high and low general learning abilities (for clarity, animals of intermediate abilities are not illustrated.) Animals
with high general learning abilities outperformed animals of low general learning abilities in each of the five
individual tasks (Lashley Maze [A], odor-guided discrimination [B], Morris Water Maze [C], fear conditioning
[D], and passive avoidance (E]). Brackets indicate standard error of the mean.
experimentally naı̈ve animals, this experiment followed the gen- fast-mapping test trial, where a novel sample stimulus was fol-
eral procedure of Experiment 1. However, at the time of testing, lowed by the subjects’ choice among a field of two familiar objects
our sample of mice was divided into two groups (with statistically (previously paired associates) and one novel object. On this test
equal general learning abilities). One group received a standard trial, a second group was exposed to a familiar sample, two
their propensity for novelty seeking or if these animals’ perfor-

p < .01
1.0
mance was indicative of fast mapping. Specifically, on the critical
test trial Group NS would be exposed to a familiar sample,
0.8 followed by a choice from among three test objects that included
Average Errors
the correct paired associate, an incorrect paired associate, and a

0.6 novel object.
On the first day of training, all 25 animals were placed in a
0.4 square open field constructed of white Plexiglas (46 ⫻ 46 ⫻ 13
cm) for 15 min. For Group FM, there were eight uniformly
0.2 distributed objects (small plastic figurines, Mattel Corp., 01-09TL)
located within the field, of which six would later be used to form
paired associates. The remaining two objects would later be used
High Intermediate Low as the critical (novel) sample and test objects. In contrast, the test
GENERAL LEARNING ABILITY
objects were absent for Group NS so that the remaining objects in
the field would be the six objects that would later form paired
Figure 3. Fast mapping test performance, Experiment 1A. Three groups associates. This initial exposure was intended to familiarize both
of animals were formed based on the upper, middle, and bottom third of the experimental and control groups to the objects that would later
factor scores (reflective of general learning performance) obtained from the constitute paired associates. By not exposing Group NS to the two
principal component analysis of learning test performance in Experiment test objects, it insured that those objects would be entirely novel at
1A. Plotted is average number of errors (⫾ standard error) on the fast the time of testing (so as to maximize any influence of novelty
mapping test trial of the animals that performed best (High), intermediate, seeking).
and worst (Low) on the battery of learning tasks. For this task, one error
On Day 2 of training, all 25 animals were acclimated to the
(on average) would be expected in a random search (assuming that re-
training apparatus (which was identical to the one used in Exper-
peated errors were not committed, in which case, the number of errors
could increase). iment 1A). Animals then underwent paired-associate training as in
Experiment 1A, and on the day following completion of this
training, the animals were again placed in the open field (as
familiar choice objects (one of which was the correct paired described above). Group NS was only exposed to the six paired-
associate), and one novel object. If the choice of the novel object associate objects and Group FM was exposed to those six objects
was directed by the animals’ propensity to choose novelty, both of as well as the two that would comprise the sample and test stimuli
the groups in this experiment should choose the novel object on on the critical test trial.
this test trial. However, if animals’ performance was guided by On the subsequent day, Group FM received a single test trial to
inferential exclusion, only animals administered the standard fast- assess their capacity for fast mapping. The fast mapping test trial
mapping test should choose the novel object. In addition to an consisted of exposure to a novel (previously unencountered in
assessment of novelty-seeking as an explanation of animals’ fast paired-associate training) sample object and a novel target object
mapping performance, Experiment 1B also served to assess the placed within a field of three objects, two of which were previous
reliability of the results described in Experiment 1A. paired associates. After exposure to the novel sample and retrieval
of the reinforcer located beneath it, the animals were allowed to
Method explore the field of three objects (two previously trained and one
novel to the test context). Target choices were then recorded until
Subjects. A new sample of 25, experimentally naı̈ve geneti- the piece of food located under the novel object was collected. For
cally heterogeneous male CD-1 outbred mice were obtained from Group NS, a previously reinforced sample object was placed in the
Harlan Laboratories (Indianapolis, IN) at 45 days of age. Housing start box and its paired associate was located within the field with
and maintenance conditions were identical to Experiment 1A. two distracter objects (a total of three objects). One of the dis-
Learning battery. Animals were first assessed in the learning tracter objects was an incorrect paired associate whereas the sec-
battery as described in Experiment 1A. Testing in the learning ond object was a novel object to which the animal had not
battery provided a second opportunity to assess the relationship previously been exposed. Target choices were recorded until the
between fast mapping performance and general learning abilities. animal chose the correct paired associate.
Furthermore, having characterized each animal’s aggregate learn-
ing performance, we were able to assign an equal distribution of
learning abilities to both of the groups represented in this experi- Results and Discussion
ment.
Fast mapping. Two weeks after the completion of the learn- A principal component analysis of the 25 animals’ performance
ing battery, the initial group of 25 animals was separated into two on the five learning tasks indicated that performance on all of the
groups which will be referred to as “Group FM” (Fast Mapping) tasks was influenced by a single source of variance (see Table 2). T2
and “Group NS” (Novelty Seeking). Group FM (n ⫽ 13) animals That factor accounted for 32% (eigenvalue 1.9) of the variance in
would undergo the fast mapping training and testing as described the animals’ performance across all learning tasks. From that
in Experiment 1A. Group NS (n ⫽ 12) would undergo a near factor analysis we were able to derive factor scores (as described
identical training and testing procedure with one critical difference above) for each individual animal. Those factor scores (which
intended to ascertain whether Group FM’s performance was due to ranged from:
10 WASS ET AL.
Table 2 mapping task was compared to their aggregate performance across

Factor Loadings From The Principal Components Analysis all learning tasks (i.e., their factor scores). That comparison re-
(n ⫽ 25) For Animals’ Performance On The Five Learning vealed a significant correlation, r(11) ⫽ .67, p ⬍ .02, which
Tasks In Experiment 1B indicates that animals with higher general learning abilities made
fewer fast mapping errors. A further analysis examining the top
General learning factor third of the distribution (animals with high GLA scores), the
Lashley III Maze ⫺.62 middle third (intermediate GLA scores) and bottom third (animals
Fear Conditioning ⫺.76 with low GLA scores) of the distribution using a one way ANOVA
Passive Avoidance ⫺.51 revealed a main effect of group F(2, 9) ⫽ 5.39, p ⬍ .03. An LSD
Odor Discrimination ⫺.32 post hoc analysis revealed a significant difference between animals
Morris Water Maze ⫺.55
of high general learning abilities and low general learning abilities,
eigenvalue 1.9
% variance .32 p ⬍ .01. No other comparisons were significant, but a trend toward
a significance was observed when animals of intermediate learning
abilities and low learning abilities were compared, p ⬍ .056. These
results are illustrated in Figure 4. F4
⫺2.39 to 1.83, where lower values indicate better aggregate
learning performance) were then used to divide the subjects into Experiment 2
two groups (Groups FM and NS) of roughly equal general learning
abilities (with an equal representation of animals of high, interme- It was established in Experiment 1A and 1B that the general
diate, and low general learning abilities). Following their assign- learning ability of mice was correlated with their performance on
ment to groups, the mean factor score of these two groups was .034 a nominal deductive reasoning (fast mapping) task. The aim of
and .048 (Groups FM and SM, respectively) and the groups did not Experiment 2 was to assess whether animals’ general learning and
differ statistically, t(23) ⫽ .03. inductive reasoning abilities were also coregulated. For this pur-
If animals’ propensity for novelty seeking determined their pose, animals that had been characterized for general learning
performance on the putative fast mapping test trial, then Group NS performance in Experiment 1A were used here (so as to compare
would be expected to choose the novel object in the test field these abilities within a single group of animals). After the com-
despite the presence of a familiar sample and test stimulus (the pletion of Experiment 1A, the animals that participated in that
correct paired associate) on the critical test trial. However, 10 out experiment were assessed on a task which could be most effi-
of the 12 animals in Group NS made no errors, choosing the ciently performed through the application of inductive reasoning.
correct paired associate test object on their first choice. Of the two To assess inductive reasoning abilities, we developed a task in
subjects that did make an error, they incorrectly chose the dis-
tracter paired associate object, not the novel test object, and then
proceeded to the correct paired associate. Of the 12 animals, 0/12
chose the novel test stimulus on either their first or second choice.
2.0 p < .01
This number of choices of the novel stimulus is below that which
would occur through even a random search, ␹2(2) ⫽ 14, p ⬍ .001,
indicating that the animals are utilizing a process that was inde-
1.5
Average Errors
pendent of novelty seeking to guide their behavior.

Unlike Group NS, Group FM was presented with both a novel
sample object and a novel test object among a field containing two
familiar objects (with a history of paired associate training). In- 1.0
ference by exclusion would dictate that under these circumstances,
animals would be disposed to choose the novel test stimulus. In
this instance, six of 13 animals chose the novel test stimulus on 0.5
their first choice, but given the relatively small sample size, this
pattern was not significantly different than chance. However, an
inspection of the subgroup of these animals with the highest
general learning scores (n ⫽ 8) revealed that these animals per- High Intermediate Low
formed well above chance levels, choosing the correct (novel) test GENERAL LEARNING ABILITY
object on six out of eight first choices (from the set of three
possible choices), ␹2(2) ⫽ 6.24, p ⬍ .05. This pattern, like that Figure 4. Fast mapping test performance, Experiment 1B. Three groups
described in Experiment 1, indicates a capacity of these animals of animals were formed based on the upper, middle, and bottom third of
for inference by exclusion. In addition, this result indicates the factor scores (reflective of general learning performance) obtained from the
principal component analysis of learning test performance in Experiment
importance of considering the performance of individual animals
1B. Plotted is average number of errors (⫾ standard error) on the fast
when assessing animals’ capacity to perform on a task that is at the mapping test trial of the animals that performed best (High), intermediate,
upper limits of their cognitive abilities. and worst (Low) on the battery of learning tasks. For this task, one error
Having demonstrated that animals’ fast mapping performance (on average) would be expected in a random search (assuming that re-
was not related to their propensity for novelty seeking, a subse- peated errors were not committed, in which case, the number of errors
quent analysis of Group FM’s performance (errors) in the fast could increase).
which animals could discern an efficient search strategy based on constructed of black Plexiglas, and a transparent sheet of Plexiglas
their experience with the overall structure of a “decision-tree” (or covered the top of the maze. The maze consisted of a start box and
F5 binary) maze (graphically represented in Figure 5). Binary trees a series of bifurcating arms. The maze bifurcated along each
are used in operations research to identify strategies that are most branch at seven symmetrically arranged locations and terminated
efficient in reaching a goal. (A colloquial version of the decision in dead ends (“leaves”). Other than at the first bifurcation (which
tree is exemplified by the process utilized to identify an object in divided the maze into two symmetric halves), each bifurcation and
the game of “20 Questions.”) Of note, this task is not simply a each leaf constituted a “node” at which a reinforcer (20 mg
maze-learning task, such as the Lashley III Maze used in the BioServe chocolate flavored pellet) could be hidden in a recessed
learning battery. In a typical egocentric maze (like the Lashley cup in the floor.
AQ: 10 Maze), the food is consistently located in a goal box and the The apparatus consisted of a start box (8 ⫻ 6 ⫻ 7 cm) located
animals learn that one path is most efficient in reaching that goal. at the base of the decision tree which was separated from the maze
Once learned, execution of a route does not involve active search- by a removable door (represented by a dashed line in Figure 5).
ing. By comparison, in this binary tree maze, both the location and Extending from the start box was the first alley of the decision tree
amount of food is randomly distributed throughout the maze at which, like all other alleys, measured 22 ⫻ 6 ⫻ 7 cm. At the end
various choice points, and there are many possible routes (of of the first alley was the first bifurcation point in which there was
varying degrees of efficiency) with which to explore the maze to no food port located. The locations of the food cups are depicted
find the available food. Thus, by design, the requirements of this in Figure 5 as dots located at each bifurcation point (except the
maze promotes the implementation of a search strategy. It is the initial bifurcation point) as well as at the end of each leaf. The food
efficacy of that strategy that will serve as our index of inductive cups were recessed holes in the base of the maze. If baited with a
reasoning. reinforce, the reinforcer would be below the level of the floor
ensuring that the animal was unable to see the reinforcer as it
Method approached the port. Each food port measure 1 cm in diameter and
Subjects. The 47 animals that served in Experiment 1A were 1.5 cm in depth. A 2 mm hole was drilled directly into the center
used here. Housing and maintenance conditions were as described of each cup which protruded through the base of the maze. This
above. hole served as an odor port for inaccessible food reinforcers (80
Decision tree maze. Two weeks following the completion of mg) that were placed beneath each food cup (to provide a uniform
Experiment 1A, animals began training in the decision tree. As distribution of olfactory cues).
depicted in Figure 5, the maze walls, floor, and doors were Forty-eight hours prior to the acclimation day the animals were
food deprived and allowed 90 min of free access to food toward
the end of their light cycle. Also, on the day prior to acclimation,
the animals were given three reinforcers to familiarize them
with the novel reinforcers to be used in the binary maze. On the
acclimation day the animals were confined to the start box for a
period of 30 sec. After 30 sec, the removable door separating the
start box from the first alley was removed, allowing the animal to
enter the maze. During this first exposure to the maze, all 14 nodes
were baited. The animal was allowed 20 min to freely navigate the
maze and find all possible reinforcers before being brought back to
the vivarium.
On 10 subsequent testing days (i.e., trials), as few as four and as
many as eight nodes were randomly baited, with a minimum of
two baited nodes on each half of the maze (all animals received the
same baited nodes). Since the actual location and number of baited
nodes varied randomly across trials, it was advantageous to the
animals to adopt a strategy for inspecting all nodes with equal
likelihood. On these critical test days, the animal was once again
confined to the start box for 30 seconds, released, and allowed to
explore the maze until all the reinforcers were retrieved and all
Figure 5. Illustration of the binary decision maze. Here, the animals’ task nodes were crossed at least once.
was to navigate the maze so as to inspect every potential node (labeled To determine if the animals had implemented a flexible search
1–14) for a payoff (a piece of food recessed in the floor). At the beginning strategy or were simply following a rote path, after the 10th day of
of each trial, food was randomly placed in 4 – 8 locations. Since the animal testing, a new procedure was instituted. Three trials were admin-
could not know the location of food or the number of goal locations that
istered (on successive days) where when an animal reached its first
were actually baited, an efficient search would inspect all nodes with
terminal leaf, the second level junction adjacent to the one occu-
minimal duplication of effort. Using an optimal search strategy, the animal
would pass a maximum of 24 nodes (as would be required were the animal pied by the animal was blocked. There were four possible locations
to search, without unnecessary duplication, every node in one half of the that could have potentially been blocked and these are represented
maze, exit that side of the maze, then search every node in the other half as dashed lines in Figure 5. As above, animals were allowed to
of the maze). continue through the maze until all food had been retrieved.
12 WASS ET AL.
To assess animal’s search efficiency, “streak” lengths were A

recorded (i.e., the number of nodes crossed prior to an animal 2
unnecessarily crossing a node that had already been visited) for r = -.46
both stages of testing (Trials 1–10 and 11–13). For the first stage
Factor Score
1
of testing (Trials 1–10), a maximally efficient search would require
24 node crossings. During the second stage (Trials 11–13), an 0
efficient search would result in 18 nodes being crossed (since one
branch was rendered inaccessible to the animals). -1
-2
Results and Discussion
4 6 8 10 12 14 16 18 20 22
In their initial 1– 4 exposures to the decision tree maze, no Average Streak (Last Four Training Trials)
systematic pattern of exploration could be detected across the B 12
group of animals or within individuals (i.e., the animals’ pattern of 10
behavior suggested a disorganized random search). However,
Average Streak
within 4 – 6 trials, the patterns of individual animals stabilized and 8
F6 remained stable for the remaining 4 days of testing (see Figure 6). 6
Although several animals performed at optimal efficiency during
the last four trials, other animals’ performance remained unsys- 4
tematic. Streak lengths ranged from 4 –24 (maximal efficiency) on 2

each of the last four trials (indicative of wide variability in ani-
mals’ performance). High Intermediate Low
The average streak length on the last four trials was compared to C
factor scores (indicative of general learning abilities) obtained
2
from the principal component analysis of learning performance r = -.56
(described in Experiment 1A). These two independent measures Factor Score
1
F7 were significantly correlated, r(45) ⫽ ⫺.46, p ⬍ .01 (Figure 7A),
indicating that the more efficient search (as indicated by longer 0
streaks) was associated with better aggregate learning abilities (as
indicated by lower factor scores). As evident in Figure 7B, the -1
streak lengths differed between animals of high, intermediate, and
low general learning abilities (the bottom, middle, and top third of -2
factor scores), F(2, 44) ⫽ 7.65, p ⬍ .001. A LSD post hoc analysis
4 6 8 10 12 14
revealed a significant difference between the streak lengths of Average Streak (Three Probe Trials)
Figure 7. Individual animals’ performance in the binary decision maze is

12 predicted by their aggregate (general) learning ability. Panel A: Factor
scores for each animal were derived from a principal component analysis
of all animals’ performance on five learning tasks. These scores reflect
animals’ aggregate performance across all five tasks. (Note that lower
10 factor scores ⫽ better aggregate learning performance.) A significant
Average Streak
correlation was observed between animals’ factor scores and the number of
node crossings prior to unnecessarily crossing a node (“streak” perfor-
mance) on the last four (of 10) test trials. Thus, the efficacy of an animal’s
8 search (a form of inductive reasoning) was predicted by their general
learning ability. Panel B: Three groups of animals were formed based on
the upper, middle, and bottom third of factor scores (reflective of general
learning performance). The average streak length (indicative of search
6
efficacy) differed across these three groups. Plotted is the animals that
performed best (High), intermediate, and worst (Low) on the battery of
1 2 3 4 5 6 7 8 9 10
learning tasks. Brackets indicate standard errors. Panel C: After an animal
reached its first low-level terminal node, the adjacent entry point was
Trials
blocked with a sliding door. This was intended to disrupt any rote path (i.e.,
algorithmic strategy) that an animal may have developed in lieu of com-
Figure 6. Performance in the binary decision tree. Plotted is the average
prehension of the overall structure of the maze. Plotted is the average streak
streak length of all 47 animals tested in this maze, where a streak of 24
during three such probe trials against factor scores obtained from the
would reflect optimal efficiency. Animals’ performance was initially er-
principal component analysis of learning performance. (Note that lower
ratic, but stabilized within six trials and remained stable thereafter. Al-
factor scores ⫽ better aggregate learning performance.) Again, a signifi-
though several animals performed at optimal efficiency during the last four
cant correlation between general learning abilities and search efficacy was
trials, other animals exhibited unsystematic performance. Streak lengths
observed.
(across animals) ranged from 4 –24 on each of the last four trials. Brackets
indicate standard error of the mean.
animals of low general learning abilities and animals of either may directly relate to the animal’s performance in a foraging task
intermediate or high abilities, p ⬍ .01. No difference in streak and have obvious and direct implications for survival in more
length was observed between animals of high and intermediate ethologically relevant environments.
learning abilities. Upon completion of Experiment 2, an additional principal com-
Following the initial 10 trials, we determined if animals were ponent analysis was conducted that included the learning data
relying on rote paths through the maze or whether they were reported in Experiment 1A, fast mapping performance from Ex-
engaging in an active search of the maze (a requisite for inductive periment 1A, and decision tree performance from Experiment 2.
reasoning). To make this determination, each animal was allowed (Data from Experiment 1B was not included in this analysis as it
to begin its exploration of the maze, and upon making its first entry was obtained from a separate sample of animals that were not
into a second level branch, the adjacent branch was blocked by assessed in the decision tree maze.) Only animals (n ⫽ 41) that
lowering a black guillotine door. Had an animal been following a contributed to both the fast mapping task (Experiment 1A) and the
rote (but nominally efficient) path through the maze, this manip- decision tree task (Experiment 2) were included in this analysis. A
ulation would have disrupted the utilization of that rote path. single factor accounted for 27% (eigan value ⫽ 1.92) of the
Animals’ streak lengths under these conditions were assessed on variance across all performance measures, and performance on
three trials. Despite the imposed disruption of the path, the corre- both the decision tree and fast mapping tasks loaded moderately
lation between the animals’ average streak and factor scores (ag- and in the same direction as performance on all of the learning
gregate learning performance) was still strong, r(45) ⫽ ⫺.56, p ⬍ tasks (see Table 3). This analysis suggests that a single underlying T3
.01 (Figure 7C). The average streak lengths for these three trials source of variance influences performance on all of these diverse
differed between animals of high, intermediate, and low general cognitive tasks.
learning abilities, F(2, 44) ⫽ 9.44, p ⬍ .001 (means ⫾ sem ⫽
10.2 ⫾ 0.86, 7.9 ⫾ 0.68, and 6.0 ⫾ .42, respectively, where a General Discussion
perfect streak ⫽ 18). LSD post hoc analysis revealed a significant
difference between animals of high and intermediate abilities, p ⬍ Over a century ago, Spearman reported the existence of a
.02, as well as between animals of high and low abilities, p ⬍ .001. general intelligence factor in humans (Spearman, 1904). The con-
Lastly, a significant difference between animals of intermediate cept of general intelligence has facilitated studies of individual
and low abilities was observed, p ⬍ .05. differences in the expression of this ubiquitous cognitive trait
The degree to which an animal can devise an efficient strategy (Jensen, 1998). Recent work with nonhuman animals has impli-
to search a maze in which the location and number of reinforcers cated the existence of a general learning ability in genetically
continuously changes is at least nominally indicative of inductive heterogeneous mice, as well as individual variations in this trait
reasoning. While numerous search strategies may be utilized to (Galsworthy et al., 2002; Kolata, Light, Grossman, Hale, & Mat-
navigate this maze, one search strategy in particular, the depth-first zel, 2007; Kolata et al., 2005; Locurto et al., 2003; Matzel et al.,
search, would be the most efficient. Other search strategies such as 2006). Although it has been asserted that this general learning
the breadth-first search or random searching would be relatively ability mice is psychometrically and structurally analogous to
inefficient strategies owing to their necessitating unnecessary node “intelligence” in humans (Kolata et al., 2008; see Blinkhorn, 2003,
crossings. It should be noted that performance in this task should for commentary), it was not previously known whether general
not be considered to be exclusively an expression of a learned learning abilities in mice were coregulated with the animals’
route, as of the various number of routes that could be learned, no capacity for reasoning. Since reasoning is considered a central
single route is most efficacious, and furthermore, would be se- function of intelligent behavior, here we aimed to address this
verely disrupted by blocking the animals’ path. Also, throughout issue, using tasks based on ones that are often asserted to reflect
this task the number of reinforcers available as well as the loca- the capacity of humans for reasoning.
tions of the reinforcers varied each day, ensuring that the animal Human reasoning abilities have been found to be highly predic-
wasn’t learning fixed reinforcer locations. These manipulations, tive of a person’s general intelligence. It is in this regard the
therefore, tested an animal’s ability to implement an efficient
search strategy in an environment that was explicitly unstable.
We have suggested that a more intelligent animal would be able Table 3
to form a more complete representation of the structure and re- Factor Loadings From The Principal Components Analysis
quirements of the maze, and would thereby implement a more (n ⫽ 41) For Performance On The Five Learning Tasks As Well
efficient search strategy. It should also be noted that other factors As Fast Mapping Performance (Experiment 1A) and The Average
such as the efficacy of an animal’s working memory may have Streak Length In The Decision Tree Maze (Experiment 2)
influenced their performance in this task. Working memory spe-
General cognitive factor
cifically has been shown to correlate with general learning abilities
in mice as well as in humans (Buehner, Krumm, & Pick, 2005; Lashley III Maze ⫺.23
Engle et al., 1995; Kolata et al., 2005, 2008; Light et al., 2010; Fear Conditioning ⫺.55
Sub, Oberauer, Wittman, Wilhelm, & Schulze, 2002). However, Passive Avoidance ⫺.28
Odor Discrimination ⫺.8
the implementation of an efficient search strategy in this task Morris Water Maze ⫺.68
would minimize any reliance on working memory. It is also Decision Tree ⫺.49
recognized that performance in this maze would be described in Fast Mapping ⫺.31
other contexts as a form of “foraging” (for review, see Rashotte, eigenvalue 1.92
% variance .27
O’Connel, & Djuric, 1985). Thus, an animal’s reasoning abilities
14 WASS ET AL.
Raven’s Progressive Matrix (RPM) test has been asserted to be one that performance on any particular task is exclusively indicative of
of the purest measures of general intelligence (Babcock, 1994; Fry the implementation of reasoning. Rather, the rationale for the
& Hale, 1996; Dawson, Soulieres, Gernsbacher, & Mottron, 2007; present experiments was that if performance by humans on a task
Jensen, 1998), and has largely supplanted many historically prev- (e.g., fast mapping) is said to rely on reasoning, than the same
alent adult intelligence tests. The RPM measures one’s ability to description can be applied to the analogous performance of a
infer rules, think rationally, reason by analogy, and to organize nonhuman animal. Our goal was not to unequivocally demonstrate
spatial information into related wholes. Therefore, if the purest the capacity for reasoning in laboratory mice, but rather, to deter-
measure of human general intelligence was based on one’s ability mine if performance on tasks that are attributed to reasoning (as
to reason, and nonhuman animals’ general learning abilities were they would be when performed by humans) are predicted by the
in fact indicative of intelligence, it would follow that the reasoning general learning abilities of these animals.
and general learning abilities of mice should be positively corre- The findings of the current study indicate that nonhuman ani-
lated. mals are indeed capable of behaviors that are at least nominally
Following Aristotle, it is often asserted that reasoning can take
indicative of various forms of reasoning (also see Blaisdell, Sawa,
one of two general forms. In the first, one attempts to understand
Leising, & Waldmann, 2006; Dusek & Eichenbaum, 1997; Pov-
the “whole” by considering only the component parts. In the
inelli, 2000; Pilley & Reid, 2011). More relevant to our present
second, one attempts to characterize a class of objects by consid-
purpose, the efficacy with which mice performed on the two
ering the common features of each object in that set. To assess
reasoning tasks reported here was directly predicted by their ag-
reasoning in laboratory mice, we devised two novel tasks which
reflect each of these forms of rational behavior. First, animals’ gregate performance across a battery of five diverse learning tasks.
performance was assessed on a fast mapping task. Fast mapping is These observations support the hypothesis that reasoning and
a mental process whereby a new concept can be learned based on general learning abilities of mice are the mutual expression of a
a logical inference derived from a single exposure to incomplete core cognitive ability that among humans would be described as
information. This corresponds with what is described as “deduc- “intelligence.”
tive” reasoning, that is, an attempt to characterize a class of objects The observation here that reasoning and general learning abili-
by considering the common features of each object in that set. Fast ties are correlated should be considered in light of previous ob-
mapping is believed to play a critical role in the extraordinarily servations that the general learning abilities of mice are predicted
rapid and seemingly effortless acquisition of information during by variations in selective attention and working memory capacity
early human development, and explains (in part) the prodigious (Kolata et al., 2005, 2008; for review, see Matzel & Kolata, 2010;
rate at which children gain vocabulary (Carey & Bartlett, 1978). In for analogous results from tests of humans, see Halford, Cowan, &
addition to fast mapping, animals’ performance was assessed in a Andrews, 2007; Unsworth & Engle, 2007). To return to one of the
“decision” or binary-tree maze. Decision trees are commonly used definitions of intelligence provided above, concepts of “intelli-
in operations research, specifically in decision analysis, to identify gence” are attempts to classify “the ability to understand complex
strategies that are most efficient in reaching a goal. While many ideas, to adapt effectively to the environment, to learn from expe-
search strategies (or paths) could be utilized to visit every node in rience, to engage in various forms of reasoning, to overcome
the decision tree, the vast majority of these paths would lead to an obstacles by taking thought.” While this and similar definitions
inefficient search, that is, one which unnecessarily retraces paths were conceived to describe a human cognitive trait, this same
or crosses goals that had already been explored. Thus, the degree definition appears relevant in summarizing the performance of
to which an animal can comprehend the whole structure of the mice on this diverse set of cognitive tasks. Thus, like humans, mice
maze and implement that information from its current location appear to express individual variations in intelligence, and these
would be a reflection of a type of “inductive” reasoning. variations have profound functional consequences for the animals’
Given the focus of the present work on what is described as the negotiation of their environments. Overall, our observation of the
capacity for “reasoning” by mice, it should be acknowledged that
coregulation of diverse cognitive abilities in mice suggests that
more elemental psychological processes (e.g., associative learning)
the operations of intelligence may have been evolutionarily
have been proposed to underlie other apparent instances of rea-
conserved across distant mammalian species (see also Banerjee
soning in nonhuman animals (Dwyer, Starns, & Honey, 2009;
et al., 2010).
Haselgrove, 2010; see Shettleworth, 2010 for relevant discussion;
It is worth noting that subregions of the prefrontal cortex may
but see Lazareva & Wasserman, 2006 for response). Similar ex-
planations (devoid of reference to reasoning) could be applied to mediate “intelligence” through their regulation of attentional con-
many instances of presumed reasoning by humans. We concede trol and/or working memory capacity (Durstewitz, Seaman, &
that what might nominally be described as “reasoning” may, at Sejnowski, 2000; Kolata et al., 2010; Sawaguchi & Goldman-
least in some instances, actually be the product of more elemental Rakic, 1991; Thurley, Senn, & Luscher, 2008; for review, see
processes. Were this the case, the relationship between human Matzel & Kolata, 2010). In fact, Kolata et al. (2010) have reported
learning abilities and intelligence (as indexed by reasoning-based that a cluster of dopamine D1-related genes in the prefrontal cortex
psychometric tests) may reflect the correlation of two traits that are are overexpressed in animals of high versus low general learning
dependent on the same (or related) underlying processes (e.g., abilities. Since general learning abilities, attentional control, and
associative learning). The same may be true in the present case, reasoning abilities appear to be coregulated, it is tempting to
where we have concluded that animals’ performance (on the fast speculate that dopaminergic signaling in the prefrontal cortex
mapping and decision tree tasks) is dependent, at least in part, on might serve as one of the (among potentially other) determinants
forms of reasoning. In this regard, it was not our intention to argue of variations in intelligence.
References modal matching to sample by a chimpanzee (pan troglodytes): compar-

ison with visual-visual intramodal matching. Animal Cognition, 4, 23–
Babcock, R. L. (1994). Analysis of adult age differences on the raven’s 239.
advanced progressive matrices test. Psychology and Aging, 9, 303–314. Jensen, A. R. (1989). The relationship between learning and intelligence.
doi:10.1037/0882-7974.9.2.303 Learning and Individual Differences, 1, 37– 62. doi:10.1016/1041-
Banerjee, K., Chabris, C. F., Johnson, V. E., Lee, J. J., Tsao, F., & Hauser, 6080(89)90009-5
M. D. (2010). General intelligence in another primate: Individual dif- Jensen, A. R. (1998). The g factor: The science of mental ability. West
ferences across cognitive task performance in a New World monkey Port, CT: Praeger.
(Saguinus oedipus). PLoS ONE, 4, e5883–5894. doi:10.1371/ Kaminski, J., Call, J., & Fischer, J. (2004). Word learning in a domestic
journal.pone.0005883 dog: Evidence for “fast mapping.” Science, 304, 1682–1683. doi:
Blaisdell, A. P., Sawa, K., Leising, K. J., & Waldmann, M. R. (2006). 10.1126/science.1097859
Causal reasoning in rats. Science, 311, 1020 –1022. doi:10.1126/ Kant, I. (1998). Critique of pure reason. New York, NY: Cambridge
science.1121872 University Press. AQ: 13
Blinkhorn, S. (2003). Of mice and mentality. Nature, 424, 1004 –1005. Kolata, S., Light, K., Grossman, H., Hale, G., & Matzel, L. D. (2007).
doi:10.1038/4241004a Selective attention is a primary determinant of the relationship between
Boysen, S. T., Berntson, G. G., Shreyer, T. A., & Quigley, K. S. (1993). working memory and general learning ability in outbred mice. Learning
Processing of ordinality and transitivity by chimpanzees. Journal of and Memory, 14, 22–28. doi:10.1101/lm.408507
Comparative Psychology, 107, 208 –215. doi:10.1037/0735-7036 Kolata, S., Light, K., & Matzel, L. D. (2008). Domain-specific and
.107.2.208 domain-general learning factors are expressed in genetically heteroge-
Buehner, M., Krumm, S., & Pick, M. (2005). Reasoning ⫽ working
neous CD-1 mice. Intelligence, 36, 619 – 639. doi:10.1016/j.intell
memory ⫽ attention. Intelligence, 33, 251–272. doi:10.1016/
.2007.12.001
j.intell.2005.01.002
Kolata, S., Light, K., Townsend, D. A., Hale, G., Grossman, H. C., &
Carey, S., & Bartlett, E. (1978). Acquiring a single new word. Proceedings
Matzel, L. D. (2005). Variations in working memory capacity predict
of the Stanford Child Language Conference, 15, 17–29.
individual differences in general learning abilities among genetically
Conway, A. R., Kane, M. J., & Engle, R. W. (2003). Working memory
diverse mice. Neurobiology of Learning and Memory, 84, 241–246.
capacity and its relation to general intelligence. Trends in Cognitive
doi:10.1016/j.nlm.2005.07.006
Sciences, 7, 522–547. doi:10.1016/j.tics.2003.10.005
Kolata, S., Light, K., Wass, C. D., Colas-Zelin, D., Roy, D., & Matzel,
Dawson, M., Soulieres, I., Gernsbacher, M. A., & Mottron, L. (2007). The
L. D. (2010). A dopaminergic gene cluster in the prefrontal cortex
level and nature of autistic intelligence. Psychological Science, 18,
predicts performance indicative of general intelligence in genetically
657– 662. doi:10.1111/j.1467-9280.2007.01954.x
heterogeneous mice. PLoS. One, 5, e14036. doi:10.1371/journal
Durstewitz, D., Seamans J. K., & Sejnowski, T. J. (2000). Dopamine-
.pone.0014036
mediated stabilization of delay-period activity in a network model of
Lazareva, O. F., & Wasserman, E. A. (2006). Effect of stimulus orderabil-
prefrontal cortex. Journal of Neurophysiology, 83, 1733–1750.
ity and reinforcement history on transitive responding in pigeons. Be-
Dusek, J. A., & Eichenbaum, H. (1997). The hippocampus and memory for
havioural Processes, 72, 161–172. doi:10.1016/j.beproc.2006.01.008
orderly stimulus relations. The National Academy of Sciences, 94, 7109 –
7114. doi:10.1073/pnas.94.13.7109 Light, K., Kolata, S., Denman-Brice, A., Zagalsky, R., & Matzel, L. D.
Dwyer, D. M., Starns, J., & Honey, R. C. (2009). “Causal reasoning” in (2010). Working memory training promotes general cognitive abilities
rats: A reappraisal. Journal of Experimental Psychology: Animal Behav- in genetically heterogeneous mice. Current Biology, 20, 777–782. doi:
ior Processes, 35, 578 –586. doi:10.1037/a0015007 10.1016/j.cub.2010.02.034
Engle, R. W., Laughlin, J. E., Tuholski, S. W., & Conway, A. R. A. (1999). Locurto, C., Fortin, E., & Sullivan, R. (2003). The structure of individual
Working memory, short-term memory, and general fluid intelligence: A differences in heterogeneous stock mice across problem types and mo-
latent variable approach. Journal of Experimental Psychology, 128, tivational systems. Genes Brain Behav, 2, 40 –55. doi:10.1034/j.1601- AQ: 14
309 –331. doi:10.1037/0096-3445.128.3.309 183X.2003.00006.x
Fry, A. F., & Hale, S. (1996). Processing speed, working memory, and MacWhinney, B. (1999). The emergence of language. Mahwah, NJ: Law-
fluid intelligence: Evidence for a developmental cascade. Psychological rence Erlbaum. AQ: 15
Science, 7, 237–241. doi:10.1111/j.1467-9280.1996.tb00366.x Manktelow, K. (1999). Reasoning and thinking. East Essex, UK: Psychol-
Galsworthy, M. J., Paya-Cano, J. L., Monleón, S., & Plomin, R. (2002). ogy Press Ltd.
Evidence for general cognitive ability (g) in heterogeneous stock mice Matzel, L. D., Grossman, H., Light, K., Townsend, D. A., & Kolata, S.
and an analysis of potential confounds. Genes, Brain, & Behavior, 11, (2008). Variations in age-related declines in general cognitive abilities of
88 –95. doi:10.1034/j.1601-183X.2002.10204.x Balb/C mice are associated with disparities in working memory span/
Gathercole, S. E., & Baddeley, A. D. (1989). Evaluation of the role of capacity and body weight. Learning and Memory, 15, 733–746. doi:
phonological STM in the development of vocabulary in children, a 10.1101/lm.954808
longitudinal study. Journal of Memory and Language, 28, 200 –213. Matzel, L. D., Han, Y. R., Grossman, H., Karnik, M. S., Patel, D., Scott,
AQ: 11 doi:10.1016/0749-596X(89)90044-2 N., et al. (2003). Individual differences in the expression of a “general” AQ: 16
Gettinger, M. (1984). Individual differences in time needed for learning: A learning ability in mice. Journal of Neuroscience, 23, 6423– 6433.
review of literature. Educational Psychologist, 19, 15–29. doi:10.1080/ Matzel, L. D., Light, K. R., Wass, C., Colas-Zelin, D., Denman-Brice, A.,
00461528409529278 Waddel, A. C., & Kolata, S. (2011). Longitudinal attentional engage-
Halford, G. S., Cowan, N., & Andrews, G. (2007). Separating cognitive ment rescues mice from age-related cognitive declines and cognitive
AQ: 12 capacity from knowledge: A new hypothesis. Trends Cogn Sci, 11, inflexibility. Learning and Memory, 18, 345–356. doi:10.1101/
236 –242. doi:10.1016/j.tics.2007.04.001 lm.2034711
Haselgrove, M. (2010). Reasoning rats or associative animals? A common- Matzel, L. D., & Kolata, S. (2010). Selective attention, working memory,
element analysis of the effects of additive and subadditive pretraining on and animal intelligence. Neuroscience and Biobehavioral Reviews, 34,
blocking. Journal of Experimental Psychology: Animal Behavior Pro- 23–30. doi:10.1016/j.neubiorev.2009.07.002
cesses, 36, 296 –306. doi:10.1037/a0016603 Matzel, L. D., Townsend, D. A., Grossman, H., Han, Y. R., Hale, G.,
Hashiya, K., & Kojima, S. (2001). Acquisition of auditory-visual inter- Zappulla, M., et al. (2006). Exploration in outbred mice covaries with AQ: 17
16 WASS ET AL.
general learning abilities irrespective of stress reactivity, emotionality Sub, H. M., Oberauer, K., Wittmann, W. W., Wilhelm, O., & Schulze, R.
and physical attributes. Neurobiology of Learning and Memory, 82, (2002). Working memory capacity explains reasoning ability and a little
228 –240. doi:10.1016/j.nlm.2006.03.004 bit more. Intelligence, 30, 261–288. doi:10.1016/S0160-2896(01)
McGonigle, B. O., & Chalmers, M. (1977). Are monkeys logical? Nature, 00100-3
246, 694 – 696. doi:10.1038/267694a0 Thurley, K., W. Senn, & H. R. Luscher. (2008). Dopamine increases the
Pilley, J. W., & Reid, A. K. (2011). Border collie comprehends object gain of the input-output response of rat prefrontal pyramidal neurons.
names as verbal referents. Behavioural Processes, 86, 184 –195. doi: Journal of Neurophysiology, 99, 2985–2997. doi:10.1152/jn.01098.2007
10.1016/j.beproc.2010.11.007 Unsworth, N., & Engle, R. W. (2000). On the division of short-term and
Povinelli, D. J. (2000). Folk Physics for Apes. New York, NY: Oxford working memory: An examination of simple and complex span and their
University Press. relation to higher order abilities. Psychological Bulletin, 133, 1038 –
Rapp, P. R., Kansky, M. T., & Eichenbaum, H. (1996). Learning and 1066. doi:10.1037/0033-2909.133.6.1038 AQ: 19
memory for hierarchical relationships in the monkey: Effects of aging.
Unsworth, N., & Engle, R. W. (2007). On the division of short-term and
Behavioral Neuroscience, 110, 887– 897. doi:10.1037/0735-
working memory: An examination of simple and complex span and their
7044.110.5.887
relation to higher order abilities. Psychological Bulletin, 133, 1038 –
Rashotte, M. E., O’Connel, J. M., & Djuric, V. J. (1985). Quantitative
1066. doi:10.1037/0033-2909.133.6.1038
Analysis of Behavior (Vol. 6): Foraging. Hillsdale, NJ: Erlbaum.
Williams, B. A., & Pearlberg, S. L. (2006). Learning of three-term con-
Roberts, W. A., & Phelps, M. T. (1994). Transitive inference in rats: A test
of the spatial coding hypothesis. Psychological Science, 5, 368 –374. tingencies correlate with Raven scores, but not with measures of cog-
doi:10.1111/j.1467-9280.1994.tb00287.x nitive processing. Intelligence, 34, 177–191. doi:10.1016/j.intell
Sawaguchi, T., & P. S. Goldman-Rakic. (1991). D1 dopamine receptors in .2005.03.007
prefrontal cortex: Involvement in working memory. Science, 251, 947– Wynne, C. D. L. (1997). Pigeon transitive inference: Tests of simple
950. doi:10.1126/science.1825731 accounts of a complex performance. Behavioural Processes, 39, 95–112.
Shettleworth, S. J. (2010). Clever animals and killjoy explanations in doi:10.1016/S0376-6357(96)00048-4
AQ: 18 comparative psychology. Trends Cogn Sci, 14, 477– 481. doi:10.1016/
j.tics.2010.07.002
Spearman, C. (1904). General intelligence, objectively determined and Received February 18, 2011
measures. American Journal of Psychology, 15, 201–293. doi:10.2307/ Revision received November 16, 2011
1412107 Accepted November 17, 2011 䡲
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Covariation of Learning and "Reasoning" Abilities in Mice: Evolutionary

Article in Journal of Experimental Psychology Animal Behavior Processes · March 2012

Christopher Wass Kenneth Light

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Andrew Marcus Smith Louis D Matzel

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Journal of Experimental Psychology: © 2012 American Psychological Association

Covariation of Learning and “Reasoning” Abilities in Mice: Evolutionary

REASONING AND GENERAL LEARNING 3

REASONING AND GENERAL LEARNING 5

REASONING AND GENERAL LEARNING 7

A: Lashley III Maze B: Odor-Guided Discrimination

Errors to Locate Reinforcer

C: Morris Water Maze D: Fear Conditioning

80 High Aggregate Learning Abilities High Aggregate Learning Abilities

Freezing During CS (Sec)

Aggregate Learning Abilities

REASONING AND GENERAL LEARNING 9

their propensity for novelty seeking or if these animals’ perfor-

the correct paired associate, an incorrect paired associate, and a

Table 2 mapping task was compared to their aggregate performance across

pendent of novelty seeking to guide their behavior.

REASONING AND GENERAL LEARNING 11

To assess animal’s search efficiency, “streak” lengths were A

tematic. Streak lengths ranged from 4 –24 (maximal efficiency) on 2

Figure 7. Individual animals’ performance in the binary decision maze is

REASONING AND GENERAL LEARNING 13

REASONING AND GENERAL LEARNING 15

References modal matching to sample by a chimpanzee (pan troglodytes): compar-

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