Papers by Naoyuki Matsumoto
Journal of neural transmission (Vienna, Austria : 1996), Jan 21, 2017
The thalamus provides a massive input to the striatum, but despite accumulating evidence, the fun... more The thalamus provides a massive input to the striatum, but despite accumulating evidence, the functions of this system remain unclear. It is known, however, that the centromedian (CM) and parafascicular (Pf) nuclei of the thalamus can strongly influence particular striatal neuron subtypes, notably including the cholinergic interneurons of the striatum (CINs), key regulators of striatal function. Here, we highlight the thalamostriatal system through the CM-Pf to striatal CINs. We consider how, by virtue of the direct synaptic connections of the CM and PF, their neural activity contributes to the activity of CINs and striatal projection neurons (SPNs). CM-Pf neurons are strongly activated at sudden changes in behavioral context, such as switches in action-outcome contingency or sequence of behavioral requirements, suggesting that their activity may represent change of context operationalized as associability. Striatal CINs, on the other hand, acquire and loose responses to external ev...
The Journal of Neuroscience, 2004
To achieve a goal, animals procure immediately available rewards, escape from aversive events, or... more To achieve a goal, animals procure immediately available rewards, escape from aversive events, or endure the absence of rewards. The neuronal substrates for these goal-directed actions include the limbic system and the basal ganglia. In the striatum, tonically active neurons (TANs), presumed cholinergic interneurons, were originally shown to respond to reward-associated stimuli and to evolve their activity through learning. Subsequent studies revealed that they also respond to aversive event-associated stimuli such as an airpuff on the face and that they are less selective to whether the stimuli instruct reward or no reward. To address this paradox, we designed a set of experiments in which macaque monkeys performed a set of visual reaction time tasks while expecting a reward, during escape from an aversive event, and in the absence of a reward. We found that TANs respond to instruction stimuli associated with motivational outcomes (312 of 390; 80%) but not to unassociated ones (51 ...
Proceedings of the National Academy of Sciences, 2011
Midbrain dopamine neurons signal reward value, their prediction error, and the salience of events... more Midbrain dopamine neurons signal reward value, their prediction error, and the salience of events. If they play a critical role in achieving specific distant goals, long-term future rewards should also be encoded as suggested in reinforcement learning theories. Here, we address this experimentally untested issue. We recorded 185 dopamine neurons in three monkeys that performed a multistep choice task in which they explored a reward target among alternatives and then exploited that knowledge to receive one or two additional rewards by choosing the same target in a set of subsequent trials. An analysis of anticipatory licking for reward water indicated that the monkeys did not anticipate an immediately expected reward in individual trials; rather, they anticipated the sum of immediate and multiple future rewards. In accordance with this behavioral observation, the dopamine responses to the start cues and reinforcer beeps reflected the expected values of the multiple future rewards and...
Neuroscience Research, 2004
Recent physiological and tract tracing studies revealed tight coupling of the centre médian and p... more Recent physiological and tract tracing studies revealed tight coupling of the centre médian and parafascicular nuclei (the CM-Pf complex), which are posterior intralaminar nuclei (ILN) of the thalamus, with basal ganglia circuits. These nuclei have previously been classified as part of the ascending reticulo-thalamo-cortical activating system, with studies of single neuron activity and of interruption of neuronal activity suggested that they participate in the processes of sensory event-driven attention and arousal, particularly in the context of unpredicted events or events contrary to predictions. In this article, we propose a hypothetical model that envisions that the CM-Pf complex functions in two different modes depending on the predictability of external events, i.e., one for monitoring 'top-down' biased control through the cortico-basal ganglia loop system for selecting signals for action and cognition and the other for switching from biased control to 'bottom-up' control based on the signals of salient external events. This model provides a new insight into the function of the CM-Pf complex and should lead to a better understanding of this important brain system.
Journal of Neurophysiology, 2007
Animals optimize behaviors by predicting future critical events based on histories of actions and... more Animals optimize behaviors by predicting future critical events based on histories of actions and their outcomes. When behavioral outcomes like reward and aversion are signaled by current external cues, actions are directed to acquire the reward and avoid the aversion. The basal ganglia are thought to be the brain locus for reward-based adaptive action planning and learning. To understand the role of striatum in coding outcomes of forthcoming behavioral responses, we addressed two specific questions. First, how are the histories of reward and aversion used for encoding forthcoming outcomes in the striatum during a series of instructed behavioral responses? Second, how are the behavioral responses and their instructed outcomes represented in the striatum? We recorded discharges of 163 presumed projection neurons in the striatum while monkeys performed a visually instructed lever-release task for reward, aversion, and sound outcomes, whose occurrences could be estimated by their histo...
Journal of Neurophysiology, 2012
Decisions maximizing benefits involve a tradeoff between the quantity of a reward and the cost of... more Decisions maximizing benefits involve a tradeoff between the quantity of a reward and the cost of elapsed time until an animal receives it. The estimation of long-term reward values is critical to attain the most desirable outcomes over a certain period of time. Reinforcement learning theories have established algorithms to estimate the long-term reward values of multiple future rewards in which the values of future rewards are discounted as a function of how many steps of choices are necessary to achieve them. Here, we report that presumed striatal projection neurons represent the long-term values of multiple future rewards estimated by a standard reinforcement learning model while monkeys are engaged in a series of trial-and-error choices and adaptive decisions for multiple rewards. We found that the magnitude of activity of a subset of neurons was positively correlated with the long-term reward values, and that of another subset of neurons was negatively correlated throughout the...
Journal of Neurophysiology, 1999
Neurons in the primate striatum and the substantia nigra pars compacta change their firing patter... more Neurons in the primate striatum and the substantia nigra pars compacta change their firing patterns during sensory-motor learning. To study the consequences of nigrostriatal dopamine depletion for learning and memory of motor sequences, we used a neurotoxin, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP), to deplete dopamine unilaterally in the striatum of macaque monkeys either before or after training them on sequential push-button motor tasks. We compared the monkeys’ performance with the arms ipsilateral and contralateral to dopamine depletion. During training and retraining on the tasks, we measured initial and serial movement times and reaction times for the push button movements, electromyographic patterns of arm and orofacial muscle activity during button pushing and reward licking, and saccadic eye movements during the button push sequences. With the arm ipsilateral to the side of dopamine depletion, each monkey showed progressive shortening of movement times and initi...
Journal of Neurophysiology, 2001
The projection from the thalamic centre médian–parafascicular (CM-Pf) complex to the caudate nucl... more The projection from the thalamic centre médian–parafascicular (CM-Pf) complex to the caudate nucleus and putamen forms a massive striatal input system in primates. We examined the activity of 118 neurons in the CM and 62 neurons in the Pf nuclei of the thalamus and 310 tonically active neurons (TANs) in the striatum in awake behaving macaque monkeys and analyzed the effects of pharmacologic inactivation of the CM-Pf on the sensory responsiveness of the striatal TANs. A large proportion of CM and Pf neurons responded to visual (53%) and/or auditory beep (61%) or click (91%) stimuli presented in behavioral tasks, and many responded to unexpected auditory, visual, or somatosensory stimuli presented outside the task context. The neurons fell into two classes: those having short-latency facilitatory responses (SLF neurons, predominantly in the Pf) and those having long-latency facilitatory responses (LLF neurons, predominantly in the CM). Responses of both types of neuron appeared regard...
PloS one, 2014
Arterial stiffness might be related to trunk flexibility in middle-aged and older participants, b... more Arterial stiffness might be related to trunk flexibility in middle-aged and older participants, but it is also affected by age, sex, and blood pressure. This cross-sectional observational study investigated whether trunk flexibility is related to arterial stiffness after considering the major confounding factors of age, sex, and blood pressure. We further investigated whether a simple diagnostic test of flexibility could be helpful to screen for increased arterial stiffening. According to age and sex, we assigned 1150 adults (male, n = 536; female, n = 614; age, 18-89 y) to groups with either high- or poor-flexibility based on the sit-and-reach test. Arterial stiffness was assessed by cardio-ankle vascular index. In all categories of men and in older women, arterial stiffness was higher in poor-flexibility than in high-flexibility (P<0.05). This difference remained significant after normalizing arterial stiffness for confounding factors such as blood pressure, but it was not foun...
Neuroscience Research, 2010
a specific strategy such as integration of visualspatioal cognition and object perception to solv... more a specific strategy such as integration of visualspatioal cognition and object perception to solve the VDMT.
International Congress Series, 2003
Although a critical involvement of dopamine has been implicated in the functions of the basal gan... more Although a critical involvement of dopamine has been implicated in the functions of the basal ganglia, especially in learning, little is known about its mechanisms. In two macaque monkeys, the nigrostriate dopamine system was unilaterally depleted by neurotoxin, 1-methyl-4-phenyl-1,2,3,6tetrahydropyridine (MPTP). We asked the monkeys to learn sequential button press tasks. In addition to the slowness of movement, they showed specific deficits in learning action strategy and reward prediction when using contralateral arm to the dopamine depletion, but with ipsilateral arm, they learned the tasks efficiently. Activity of single, midbrain dopamine neurons was recorded from two monkeys in a task in which they chose one correct, rewarding button among three alternatives in a trial and error basis. It was found that the magnitudes of responses to beep sound informing correct and incorrect choices precisely reward prediction error signals. We present a hypothetical scheme for the mechanisms of action learning in the basal ganglia, in which the nigrostriate dopamine system provides the striatum, locus of learning, with reward prediction errors as a teaching signal for learning, and excitability of the striate projection neurons to specific cortical inputs is modified by the teaching signal so as to achieve goal-directed action selection.
Experimental Brain Research, 2011
Behavioral decisions and actions are directed to achieve specific goals and to obtain rewards and... more Behavioral decisions and actions are directed to achieve specific goals and to obtain rewards and escape punishments. Previous studies involving the recording of neuronal activity suggest the involvement of the cerebral cortex, basal ganglia, and midbrain dopamine system in these processes. The value signal of the action options is represented in the striatum, updated by reward prediction errors, and used for selecting higher-value actions. However, it remains unclear whether dysfunction of the striatum leads to impairment of value-based action selection. The present study examined the effect of inactivation of the putamen via local injection of the GABA A receptor agonist muscimol in monkeys engaged in a manual reward-based multi-step choice task. The monkeys first searched a reward target from three alternatives, based on the previous one or two choices and their outcomes, and obtained a large reward; they then earned an additional reward by choosing the last rewarded target. Inactivation of the putamen impaired the ability of monkeys to make optimal choices during third trial in which they were required to choose a target different from those selected in the two previous trials by updating the values of the three options. The monkeys normally changed options if the last choice resulted in small reward (lose-shift) and stayed with the last choice if it resulted in large reward (win-stay). Task start time and movement time during individual trials became longer after putamen inactivation. But monkeys could control the motivation level depending on the reward value of individual trial types before and after putamen inactivation. These results support a view that the putamen is involved selectively and critically in neuronal circuits for reward history-based action selection. Keywords Putamen Á Muscimol Á Reward Á Reinforcement learning Á Decision-making Manabu Muranishi and Hitoshi Inokawa contributed equally to this work.
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Papers by Naoyuki Matsumoto