Autobiographical Odor Memory

INTERNATIONAL SYMPOSIUM ON OLFACTION AND TASTE Autobiographical Odor Memory Maria Larsson and Johan Willander Department of Psychology, Stockholm University, Stockholm, Sweden This overview focuses on autobiographical odor memory and how information evoked by the olfactory sense may differ from memories evoked by visual or verbal information. Three key topics are addressed: (a) age distributions of evoked memories; (b) phenomenological experience; and (c) semantic processing. Current evidence suggests that memories triggered by olfactory information are localized to the first decade of life (< 10 years) rather than to young adulthood (10–30 years) which is the typical finding for memories evoked by verbal and visual information. Further, empirical evidence indicates that odor evoked memories are more emotional, associated with stronger feelings of being brought back in time, and have been thought of less often as compared to memories evoked by other sensory cues. Finally, previous observations of a significant impact of semantic influences on olfactory processing may also be generalized to retrieval of odor evoked autobiographical information. Specifically, both the age distribution and phenomenological qualities are affected by explicit knowledge of the odor cue. Taken together, the overall pattern of findings indicates that personal memories evoked by olfactory information are different from memories evoked by verbal or visual information. Key words: odor; memory; autobiographical Introduction This overview is devoted to the exploration of autobiographical odor memory and how information evoked by the olfactory sense may differ from memories evoked by visual or verbal information. Although memory scientists have focused extensively on autobiographical memory, most of the available evidence is based on verbal cuing, and evidence is sparse regarding how other cue types influence the recollection of personal events. Autobiographical memory concerns personal events from one’s life. A defining aspect is mental time travel, “episodic (i.e., autobiographical) memory does exactly what the other forms of memory do not and cannot do—it enables the individual to mentally Address for correspondence: Maria Larsson, Department of Psychology, Stockholm University, Frescati hagväg 14, SE-106 91 Stockholm, Sweden. Voice: +46 8 16 39 37; fax: +46 8 15 93 42. [email protected] travel back into her personal past” (p. 266).1 Autobiographical memories may be assessed differently depending on the specific research question. The most utilized method is the Galton-Crovitz method also known as the word-cue method.2 The procedure is as follows: participants are given a number of cues (e.g., words, pictures, odors) and asked to produce an autobiographical memory for each cue. In instances of successful retrieval, a short description of the event is provided along with experiential ratings of the retrieved event (e.g., emotionality, vividness). When all cues have been presented, the participant is asked to go back to each evoked event and to date it (i.e., to indicate the age-at-event). In the overview, we will highlight some of the available empirical observations focusing on autobiographical odor memory. Specifically, the following topics will be addressed: (a) the age distribution of odor evoked information; (b) phenomenological experience; and (c) the role played by semantic processing. International Symposium on Olfaction and Taste: Ann. N.Y. Acad. Sci. 1170: 318–323 (2009). c 2009 New York Academy of Sciences. doi: 10.1111/j.1749-6632.2009.03934.x  318 Larsson & Willander : Autobiographical Odor Memory The Age Distribution of Autobiographical Odor Memories A central topic in autobiographical memory research concerns the age distribution of memories across the lifespan. Typically, in the investigation of age distributions, participants are asked to retrieve memories for specific cues and date them according to age at the occurrence of the event. The distribution of memories is obtained by dividing the lifespan into intervals (e.g., 5- or 10-year intervals). Two decades of autobiographical memory research have established that the age distribution of memories evoked by verbal information follows a specific pattern involving three components: the childhood amnesia, the bump, and recency or forgetting.3 Childhood amnesia reflects the dramatic reduction of memories reported from early childhood. In contrast, a substantially larger number of memories are recalled from the ages of 10–30, a phenomenon that has been termed the bump.3 The third component, recency, reflects better retention of events occurring from the last 10 years.4 However, as noted above, the available knowledge is based on verbal cuing of personal memories. To date, only a few studies have focused on the age of odor-evoked memories. In a seminal study, Rubin, Groth, and Goldsmith5 compared memories evoked by odors, photographs, and verbal labels in undergraduates and found similar age distributions for all cue types. Likewise, using a sample of young adults, Goddard, Pring, and Felmingham6 reported no differences in age distributions for words, pictures, and odors. In contrast, recent studies comprising older age cohorts have reported of a bump appearing at an earlier age for odorevoked memories (i.e., < 10 years) than for verbally cued memories (i.e., 10–30 years). Testing a smaller sample of older adults (n = 22), Chu and Downes7 presented odors or words and asked the participants to relate any autobiographical event to the respective cue. In instances when a memory was retrieved subjects also indicated the age-at-event. The results 319 showed that the bump for memories evoked by odors was located to the 6–10 year interval as compared to the label-cued events that peaked between 11 and 20 years. In two recent studies from our lab,8,9 using two larger independent samples of older adults we have reported that olfactory evoked autobiographical information indeed is older than memories evoked by verbal or visual information. In the first study,8 the test materials used were selected in such a way that each cue could be presented as a word, picture, or an odor. Ninety-three older participants (mean age 74.3 years, range 65– 80) were presented with one of the three cue types and were asked to retrieve any memory from the personal past. As shown in Figure 1, most of the memories evoked by odors were clearly located to the first decade of life (< 10 years), whereas memories associated with verbal and visual cues peaked in early adulthood (11–20 years). In a follow-up study involving 72 older adults (mean age 71.7 years, range 65–80), we replicated the finding of a significant clustering of childhood related memories for odors whereas verbally evoked memories peaked in young adulthood.9 Anecdotally, it is often stated that odors should be more potent reminders of past experiences than other sensory cues. However, a review of the scarce evidence indicates that this statement is not substantiated by experimental research. Earlier work indicated that odor cues produced fewer memories than words or pictures, and were associated with longer response latencies.5,6 Likewise, Willander and Larsson9 found that fewer memories were elicited by olfactory as compared with verbal retrieval cues. These observations suggest that olfactory cues may be less efficient reminders of past experiences than verbal ones. One potential explanation for this finding may be cue specificity. It has been suggested that odors are more specific cues than verbal or pictorial information. Odors may therefore match fewer memories than more generic cues such as words or pictures. Indeed, empirical evidence shows that if semantic information is provided with the odor 320 Annals of the New York Academy of Sciences Figure 1. Upper panel: The distribution of (A) odor-cued, (B) word-cued, and (C) picture-cued autobiographical memories across the lifespan. Lower panel: The distribution of (D) odor-only-, (E) name-only-, and (F) odor-name-evoked autobiographical memories across the lifespan. Error bars indicate ±1 standard error. cue (i.e., the odor name), more memories will be generated.8 To summarize, current evidence regarding the age distribution of autobiographical odor memory suggests that: (a) the olfactory bump is not observable for younger cohorts whereas it is for older cohort samples; (b) the bump location is not a fixed property of the age distribution of memories, but rather varies as a function of the cue type; and that (c) memories triggered by olfactory information are localized to the first decade of life (< 10 years) rather than to young adulthood. Phenomenological Experience in Odor-evoked Memories Autobiographical odor memories have been characterized on a number of experiential dimensions, such as emotion, pleasantness, vividness, and the feeling of being brought back in time to the occurrence of the event. As shown below, the available evidence portrays a mixed pattern of results with regard to phenomeno- logical experiences in autobiographical odor memory. A central aspect of olfactory processing and olfactory memory is emotion. Given that the olfactory system projects directly to the amygdala complex it has been proposed that olfactory evoked memories are more emotional than memories evoked by other cue types. The fundamental role of the amygdala in emotional processing of memories is well established.10 Most studies targeting autobiographical memories have reported an emotional advantage of olfactory evoked information over verbally and visually evoked memories,11,12 although others have failed to find support for the fact that odor memories should be experienced with a stronger emotional connotation.8,13 The latter studies demonstrated a pictorial advantage in the retrieval of emotional events. Evidence is also mixed regarding whether odors also carry the potential to evoke more vivid and detailed memories than other modalities. Chu and Downes14 compared memories evoked by olfactory and verbal cues. The results showed that autobiographical odor information was Larsson & Willander : Autobiographical Odor Memory experienced as more vivid than memories evoked by verbal labels. However, later studies do not support the notion that olfactory memory entails a more vivid recollection as compared to other sensory formats.8,9,12 The results are more stable with regard to the experience of mental time travel. Stronger feelings of being brought back to the occurrence of the events for odor-evoked events than for memories evoked by words or pictures have been reported across several studies.5,7–9,12 The underlying mechanisms for this observation are unclear. However, a potential explanation may be the close synapsing between the olfactory bulb and the hippocampus. The hippocampus is involved in the temporal processing of information and is critical for the retrieval of episodic information.15 Another critical brain region for the recollection of autobiographical information is the prefrontal cortex.16 Thus, odor cues may potentially activate the hippocampus and prefrontal regions during autobiographical memory retrieval producing stronger temporal autonoetic awareness. It is also of interest to note that memories evoked by odors in general have been thought of less often that memories evoked by other sensory cues,5,8 a phenomenon that probably underlies the experienced “suddenness” of an odorevoked memory. To conclude, the overall pattern of findings support the notion that odor-evoked memories are more emotional, associated with stronger feelings of being brought back in time, and have been thought of less often as compared to memories evoked by other cues. The Influence of Semantic Processing in Odor-evoked Memories Early research focusing on the relationship between semantic processing and episodic odor memory revealed little or no influence of verbal knowledge on memory performance.17 However, later work clearly demonstrates that ol- 321 factory perception and memory is influenced by verbal knowledge of the odor. Influences of semantic processes on a number of olfactory tasks, such as episodic recognition,18,19 odor naming,20 familiarity,21 and hedonic evaluations,22 have been established. Until recently, an unexplored question concerned whether verbal and conceptual processing has an impact on the age distributions and phenomenological experience of autobiographical odor memories. Given that autobiographical odor memory draws on episodic memory, it is of interest to explore whether verbal processes also influence the recollection of autobiographical olfactory information. Willander and Larsson9 examined the potential influence of conceptual processing on autobiographical odor memory using three retrieval conditions: a perceptual (odor-only), semantic (name-only), and a mixed condition (perceptual and semantic). As shown in the lower panel in Figure 1, the results showed that memories retrieved in the odoronly condition were localized to the first decade of life, whereas the distribution of memories evoked in the name-only condition showed a tendency to peak in young adulthood.8 In the odor-name condition, the age distribution took an intermediate position between the nameonly and odor-name distributions, with a bump localized to the first two decades of life (0– 20 years). On the basis of these findings, and on previous empirical observations,23,24 we concluded that additional semantic knowledge of an odor produces a shift in processing from a more perceptually driven to a more conceptually driven retrieval. According to Paivio’s dual code theory,25 odors are not stored in a dual code format (i.e., as a verbal and perceptual representation). Our results support this notion because if olfactory knowledge would play a fundamental role in the generation of the bump, the odor-only condition would not differ from the odor-name or name-only conditions. Therefore, it may be suggested that autobiographical memories triggered by olfactory information primarily is driven by the perceptual properties of the specific odor. 322 Annals of the New York Academy of Sciences Research suggests that different retrieval strategies may influence event selection and the age distribution of autobiographical events.26 Two retrieval modes have been suggested: strategic and automatic. In strategic retrieval, cues entail an intentional cyclic and elaborative search process of memory information until a specific memory is formed, a process that has been associated with verbal cues.27 In automatic retrieval, recollection is direct and effortless and immediately activates a representation of an event in memory. To the extent that odors presented with labels primarily were experienced as verbal items, the present observations suggest that participants in the odorname condition engaged in a more strategic retrieval process, whereas odors-only may have induced a more direct and automatic activation of sensory-specific autobiographical information. Thus, retrieval of odor-evoked memories may bypass the selection process resulting in an earlier bump location.26 However, when semantic information regarding the odor cues is available, generative retrieval may become activated. Further, the phenomenological qualities of the retrieved memories were affected by olfactory knowledge. Perceived pleasantness, emotionality, and feelings of being brought back in time were lower when odors were presented with their respective names as compared when only an odor was presented. Indeed, when participants were aware of the odor’s identity, the experiential ratings did not differ from the ones obtained by names. Taken together, previous observations of a significant impact of semantic influences on olfactory processing may also be generalized to retrieval of odor-evoked autobiographical information. Specifically, both the age distribution and phenomenological qualities were affected by explicit knowledge of the odor cue. Overall Conclusion Autobiographical memory retrieval involves the recollection of information spanning dif- ferent sensory domains. Current research indicates that the age of the evoked memories may vary significantly depending on the cue’s sensory modality. Also, evidence suggests that distinct autobiographical episodes consisting of olfactory information are formed earlier in life than are those comprising verbal and visual information. This observation supports research showing that associative odor learning begins very early in life,28 with events and experiences that ultimately may become accessible in old age through exposure to event-congruent olfactory information. Suggestions for future work include elucidation of the role played by retroactive interference in olfactory processing, the veridicality of olfactory retrieved events, and multimodal cuing of autobiographical memories. Acknowledgment This work was supported by a grant from The Swedish Research Council to M. L. (No. F0647/2001). Conflicts of Interest The authors declare no conflicts of interest. References 1. Tulving, E. 1998. 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