Episodic memory and recognition are influenced by cues' sensory modality: comparing odours, music and faces using virtual reality.

Most everyday experiences are multisensory, and all senses can trigger the conscious re-experience of unique personal events embedded in their specific spatio-temporal context. Yet, little is known about how a cue's sensory modality influences episodic memory, and which step of this process is impacted. This study investigated recognition and episodic memory across olfactory, auditory and visual sensory modalities in a laboratory-ecological task using a non-immersive virtual reality device. At encoding, participants freely and actively explored unique and rich episodes in a three-room house where boxes delivered odours, musical pieces and pictures of face. At retrieval, participants were presented with modality-specific memory cues and were told to 1) recognise encoded cues among distractors and, 2) go to the room and select the box in which they encountered them at encoding. Memory performance and response times revealed that music and faces outperformed odours in recognition memory, but that odours and faces outperformed music in evoking encoding context. Interestingly, correct recognition of music and faces was accompanied by more profound inspirations than correct rejection. By directly comparing memory performance across sensory modalities, our study demonstrated that despite limited recognition, odours are powerful cues to evoke specific episodic memory retrieval.

Personal familiarity of music and its cerebral effect on subsequent speech processing.

Despite the obvious personal relevance of some musical pieces, the cerebral mechanisms associated with listening to personally familiar music and its effects on subsequent brain functioning have not been specifically evaluated yet. We measured cerebral correlates with functional magnetic resonance imaging (fMRI) while composers listened to three types of musical excerpts varying in personal familiarity and self (familiar own/composition, familiar other/favorite or unfamiliar other/unknown music) followed by sequences of names of individuals also varying in personal familiarity and self (familiar own/own name, familiar other/close friend and unfamiliar other/unknown name). Listening to music with autobiographical contents (familiar own and/or other) recruited a fronto-parietal network including mainly the dorsolateral prefrontal cortex, the supramarginal/angular gyri and the precuneus. Additionally, while listening to familiar other music (favorite) was associated with the activation of reward and emotion networks (e.g. the striatum), familiar own music (compositions) engaged brain regions underpinning self-reference (e.g. the medial prefrontal cortex) and visuo-motor imagery. The present findings further suggested that familiar music with self-related reference (compositions) leads to an enhanced activation of the autobiographical network during subsequent familiar name processing (as compared to music without self-related reference); among these structures, the precuneus seems to play a central role in personally familiar processing.

"What-Where-Which" Episodic Retrieval Requires Conscious Recollection and Is Promoted by Semantic Knowledge.

Episodic memory is defined as the conscious retrieval of specific past events. Whether accurate episodic retrieval requires a recollective experience or if a feeling of knowing is sufficient remains unresolved. We recently devised an ecological approach to investigate the controlled cued-retrieval of episodes composed of unnamable odors (What) located spatially (Where) within a visual context (Which context). By combining the Remember/Know procedure with our laboratory-ecological approach in an original way, the present study demonstrated that the accurate odor-evoked retrieval of complex and multimodal episodes overwhelmingly required conscious recollection. A feeling of knowing, even when associated with a high level of confidence, was not sufficient to generate accurate episodic retrieval. Interestingly, we demonstrated that the recollection of accurate episodic memories was promoted by odor retrieval-cue familiarity and describability. In conclusion, our study suggested that semantic knowledge about retrieval-cues increased the recollection which is the state of awareness required for the accurate retrieval of complex episodic memories.

Lateralization of olfactory processing: differential impact of right and left temporal lobe epilepsies.

Olfactory processes were reported to be lateralized. The purpose of this study was to further explore this phenomenon and investigate the effect of the hemispheric localization of epileptogenic foci on olfactory deficits in patients with temporal lobe epilepsy (TLE). Olfactory functioning was assessed in 61 patients and 60 healthy control (HC) subjects. The patients and HC subjects were asked to rate the intensity, pleasantness, familiarity, and edibility of 12 common odorants and then identify them. Stimulations were delivered monorhinally in the nostril ipsilateral to the epileptogenic focus in TLE and arbitrarily in either the left or the right nostril in the HC subjects. The results demonstrated that regardless of the side of stimulation, patients with TLE had reduced performance in all olfactory tasks compared with the HC subjects. With regard to the side of the epileptogenic focus, patients with left TLE judged odors as less pleasant and had more difficulty with identification than patients with right TLE, underlining a privileged role of the left hemisphere in the emotional and semantic processing of odors. Finally, irrespective of group, a tendency towards a right-nostril advantage for judging odor familiarity was found in agreement with a prominent role of the right hemisphere in odor memory processing.

A review on the neural bases of episodic odor memory: from laboratory-based to autobiographical approaches.

Odors are powerful cues that trigger episodic memories. However, in light of the amount of behavioral data describing the characteristics of episodic odor memory, the paucity of information available on the neural substrates of this function is startling. Furthermore, the diversity of experimental paradigms complicates the identification of a generic episodic odor memory network. We conduct a systematic review of the literature depicting the current state of the neural correlates of episodic odor memory in healthy humans by placing a focus on the experimental approaches. Functional neuroimaging data are introduced by a brief characterization of the memory processes investigated. We present and discuss laboratory-based approaches, such as odor recognition and odor associative memory, and autobiographical approaches, such as the evaluation of odor familiarity and odor-evoked autobiographical memory. We then suggest the development of new laboratory-ecological approaches allowing for the controlled encoding and retrieval of specific multidimensional events that could open up new prospects for the comprehension of episodic odor memory and its neural underpinnings. While large conceptual differences distinguish experimental approaches, the overview of the functional neuroimaging findings suggests relatively stable neural correlates of episodic odor memory.

A unique memory process modulated by emotion underpins successful odor recognition and episodic retrieval in humans.

We behaviorally explore the link between olfaction, emotion and memory by testing the hypothesis that the emotion carried by odors facilitates the memory of specific unique events. To investigate this idea, we used a novel behavioral approach inspired by a paradigm developed by our team to study episodic memory in a controlled and as ecological as possible way in humans. The participants freely explored three unique and rich laboratory episodes; each episode consisted of three unfamiliar odors (What) positioned at three specific locations (Where) within a visual context (Which context). During the retrieval test, which occurred 24-72 h after the encoding, odors were used to trigger the retrieval of the complex episodes. The participants were proficient in recognizing the target odors among distractors and retrieving the visuospatial context in which they were encountered. The episodic nature of the task generated high and stable memory performances, which were accompanied by faster responses and slower and deeper breathing. Successful odor recognition and episodic memory were not related to differences in odor investigation at encoding. However, memory performances were influenced by the emotional content of the odors, regardless of odor valence, with both pleasant and unpleasant odors generating higher recognition and episodic retrieval than neutral odors. Finally, the present study also suggested that when the binding between the odors and the spatio-contextual features of the episode was successful, the odor recognition and the episodic retrieval collapsed into a unique memory process that began as soon as the participants smelled the odors.

Modular structure of functional networks in olfactory memory.

Graph theory enables the study of systems by describing those systems as a set of nodes and edges. Graph theory has been widely applied to characterize the overall structure of data sets in the social, technological, and biological sciences, including neuroscience. Modular structure decomposition enables the definition of sub-networks whose components are gathered in the same module and work together closely, while working weakly with components from other modules. This processing is of interest for studying memory, a cognitive process that is widely distributed. We propose a new method to identify modular structure in task-related functional magnetic resonance imaging (fMRI) networks. The modular structure was obtained directly from correlation coefficients and thus retained information about both signs and weights. The method was applied to functional data acquired during a yes-no odor recognition memory task performed by young and elderly adults. Four response categories were explored: correct (Hit) and incorrect (False alarm, FA) recognition and correct and incorrect rejection. We extracted time series data for 36 areas as a function of response categories and age groups and calculated condition-based weighted correlation matrices. Overall, condition-based modular partitions were more homogeneous in young than elderly subjects. Using partition similarity-based statistics and a posteriori statistical analyses, we demonstrated that several areas, including the hippocampus, caudate nucleus, and anterior cingulate gyrus, belonged to the same module more frequently during Hit than during all other conditions. Modularity values were negatively correlated with memory scores in the Hit condition and positively correlated with bias scores (liberal/conservative attitude) in the Hit and FA conditions. We further demonstrated that the proportion of positive and negative links between areas of different modules (i.e., the proportion of correlated and anti-correlated areas) accounted for most of the observed differences in signed modularity. Taken together, our results provided some evidence that the neural networks involved in odor recognition memory are organized into modules and that these modular partitions are linked to behavioral performance and individual strategies.

Odor mental imagery in non-experts in odors: a paradox?

In agreement with the theoretical framework stipulating that mental images arise from neural activity in early sensory cortices, the primary olfactory cortex [i.e., the piriform cortex (PC)] is activated when non-olfactory-experts try to generate odor mental images. This finding strongly contrasts with the allegation that it is typically impossible to mentally imagine odors. However, other neurophysiological or cognitive processes engaged in the endeavor of odor mental imagery such as sniffing, attention, expectation, and cross-modal interactions involve the PC and could explain this paradox. To unambiguously study the odor mental imagery, we first argued the need to investigate odor experts who have learned to specifically reactivate olfactory percepts. We then assert the necessity to explore the network dedicated to this function by considering variations in both the activity level and the connection strength of the areas belonging to this network as a function of the level of expertise of the odor experts.

A novel experimental approach to episodic memory in humans based on the privileged access of odors to memories.

Episodic memory is defined as the conscious recollection of a personal event (What) in its spatial (Where) and contextual (Which context) environment. In existing approaches, human episodic memory is either explored separately from real-life situations or is not fully controlled. In this study, we propose an intermediate approach, inspired by animal studies, that permits the control of the encoding and recall phases, while still being ecologically valid. As odors are known to be especially evocative reminders, we explored the memory of olfactory episodes. During trial-unique encoding, participants freely explored three episodes, one episode per day, each composed of three unnamable odors (What) that were positioned at specific locations on a board (Where) within a visual context (Which context). On the fourth day, both old and new odors were presented, and when an odor was recognized, the participants had to remember both its spatial location and the visual context in which it occurred. In Experiment 1, the participants were highly proficient at recognizing odors, and they recall the spatio-contextual environment associated with these odors in approximately half of the trials. To adapt the recall procedure to the constraints of fMRI, we conducted Experiment 2 demonstrating that trial repetition did not disturb the memory process. Thus, we first validated our protocol, which investigates the memory of olfactory episodes in a fully controlled way that is as close as possible to real-life situations. Then, we demonstrated the adaptability of our protocol for the future exploration of the neural networks implicated in episodic recall.

Perfumers' expertise induces structural reorganization in olfactory brain regions.

The human brain's ability to adapt to environmental changes is obvious in specific sensory domains of experts, and olfaction is one of the least investigated senses. As we have previously demonstrated that olfactory expertise is related to functional brain modifications, we investigated here whether olfactory expertise is also coupled with structural changes. We used voxel-based morphometry to compare the gray-matter volume in student and professional perfumers, as well as untrained control subjects, and accounted for all methodological improvements that have been recently developed to limit possible errors associated with image processing. In all perfumers, we detected an increase in gray-matter volume in the bilateral gyrus rectus/medial orbital gyrus (GR/MOG), an orbitofrontal area that surrounds the olfactory sulcus. In addition, gray-matter volume in the anterior PC and left GR/MOG was positively correlated with experience in professional perfumers. We concluded that the acute olfactory knowledge acquired through extensive olfactory training leads to the structural reorganization of olfactory brain areas.

The impact of expertise in olfaction.

Olfactory expertise remains poorly understood, most likely because experts in odor, such as perfumers, sommeliers, and oenologists, are much rarer than experts in other modalities, such as musicians or sportsmen. In this review, we address the specificities of odor expertise in both odor experts and in a priori untrained individuals who have undergone specific olfactory training in the frame of an experiment, such as repeated exposure to odors or associative learning. Until the 21st century, only the behavioral effects of olfactory training of untrained control individuals had been reported, revealing an improvement of olfactory performance in terms of sensitivity, discrimination, memory, and identification. Behavioral studies of odor experts have been scarce, with inconsistent or inconclusive results. Recently, the development of cerebral imaging techniques has enabled the identification of brain areas and neural networks involved in odor processing, revealing functional and structural modifications as a function of experience. The behavioral approach to odor expertise has also evolved. Researchers have particularly focused on odor mental imagery, which is characteristic of odor experts, because this ability is absent in the average person but is part of a perfumer's professional practice. This review summarizes behavioral, functional, and structural findings on odor expertise. These data are compared with those obtained using animals subjected to prolonged olfactory exposure or to olfactory-enriched environments and are discussed in the context of functional and structural plasticity.

Experience induces functional reorganization in brain regions involved in odor imagery in perfumers.

Areas of expertise that cultivate specific sensory domains reveal the brain's ability to adapt to environmental change. Perfumers are a small population who claim to have a unique ability to generate olfactory mental images. To evaluate the impact of this expertise on the brain regions involved in odor processing, we measured brain activity in novice and experienced (student and professional) perfumers while they smelled or imagined odors. We demonstrate that olfactory imagery activates the primary olfactory (piriform) cortex (PC) in all perfumers, demonstrating that similar neural substrates were activated in odor perception and imagination. In professional perfumers, extensive olfactory practice influences the posterior PC, the orbitofrontal cortex, and the hippocampus; during the creation of mental images of odors, the activity in these areas was negatively correlated with experience. Thus, the perfumers' expertise is associated with a functional reorganization of key olfactory and memory brain regions, explaining their extraordinary ability to imagine odors and create fragrances.

Alliesthesia is greater for odors of fatty foods than of non-fat foods.

Alliesthesia is the modulation of the rewarding value of a stimulus according to the internal state (hungry or satiated). This study aimed to evaluate this phenomenon as a function of the nature of the stimulus (odors evoking edible and non-edible items, and the food odors evoking fatty and non-fat foods) and to compare the effectiveness of two reward evaluations (measures of pleasantness and appetence) to reveal alliesthesia. The results showed that both fatty and non-fat food odors were judged as less pleasant and less appetent when the subjects were satiated than when they were hungry, whereas no such difference was observed for non-food odors. There was a greater decrease in appetence than there was in pleasantness. Moreover, the decrease in appetence was greater for fatty than for non-fat food odors, whereas the decrease in pleasantness was similar for both fatty and non-fat food odors. Our study allows for the definition of a more comprehensive pattern of alliesthesia based on odor category. It demonstrates that alliesthesia is specific to food odors and that it is more pronounced when odors are associated with fatty rather than non-fat foods. It also reveals that an appetence measure is more sensitive than a pleasantness measure for describing an acute reward modulation process.

True and false recognition memories of odors induce distinct neural signatures.

Neural bases of human olfactory memory are poorly understood. Very few studies have examined neural substrates associated with correct odor recognition, and none has tackled neural networks associated with incorrect odor recognition. We investigated the neural basis of task performance during a yes-no odor recognition memory paradigm in young and elderly subjects using event-related functional magnetic resonance imaging. We explored four response categories: correct (Hit) and incorrect false alarm (FA) recognition, as well as correct (CR) and incorrect (Miss) rejection, and we characterized corresponding brain responses using multivariate analysis and linear regression analysis. We hypothesized that areas of the medial temporal lobe were differentially involved depending on the accuracy of odor recognition. In young adults, we found that significant activity in the hippocampus and the parahippocampal gyrus was associated with correct (true) recognition of odors, whereas the perirhinal cortex was associated with FAs and Misses. These findings are consistent with literature regarding hypothetical functional organization for memory processing. We also found that for correct recognition and rejection responses, the involvement of the hippocampus decreased when memory performances improved. In contrast to young individuals, elderly subjects were more prone to false memories and exhibited less specific activation patterns for the four response categories. Activation in the hippocampus and the parahippocampal gyrus was positively correlated with response bias scores for true and false recognition, demonstrating that conservative subjects produced an additional search effort leading to more activation of these two medial temporal lobe regions. These findings demonstrate that correct and incorrect recognition and rejection induce distinct neural signatures.

Music lexical networks: the cortical organization of music recognition.

Successful recognition of a familiar tune depends on a selection procedure that takes place in a memory system that contains all the representations of the specific musical phrases to which one has been exposed during one's lifetime. We refer to this memory system as the musical lexicon. The goal of the study was to identify its neural correlates. The brains of students with little musical training were scanned with functional magnetic resonance imaging (fMRI) while the student listened to familiar musical themes, unfamiliar music, and random tones. The familiar themes were selected from instrumental pieces well-known to the participants; the unfamiliar music was the retrograde version of the familiar themes, which the participants did not recognize; and the random sequences contained the same musical tones but in a random order. All stimuli were synthesized and played with the sound of a piano, thereby keeping low-level acoustical factors similar across conditions. The comparison of cerebral responses to familiar versus unfamiliar music reveals focal activation in the right superior temporal sulcus (STS). Re-analysis of the data obtained in a previous study by Plailly et al. also points to the STS as the critical region involved in musical memories. The neuroimaging data further suggest that these auditory memories are tightly coupled with action (singing), by showing left activation in the planum temporale, in the supplementary motor area (SMA), and in the inferior frontal gyrus. Such a cortical organization of music recognition is analogous to the dorsal stream model of speech processing proposed by Hickok and Poeppel.

Odor quality coding and categorization in human posterior piriform cortex.

Efficient recognition of odorous objects universally shapes animal behavior and is crucial for survival. To distinguish kin from nonkin, mate from nonmate and food from nonfood, organisms must be able to create meaningful perceptual representations of odor qualities and categories. It is currently unknown where and in what form the brain encodes information about odor quality. By combining functional magnetic resonance imaging (fMRI) with multivariate (pattern-based) techniques, we found that spatially distributed ensemble activity in human posterior piriform cortex (PPC) coincides with perceptual ratings of odor quality, such that odorants with more (or less) similar fMRI patterns were perceived as more (or less) alike. We did not observe these effects in anterior piriform cortex, amygdala or orbitofrontal cortex, indicating that ensemble coding of odor categorical perception is regionally specific for PPC. These findings substantiate theoretical models emphasizing the importance of distributed piriform templates for the perceptual reconstruction of odor object quality.

Attention to odor modulates thalamocortical connectivity in the human brain.

It is widely assumed that the thalamus is functionally irrelevant for the sense of smell. Although animal studies suggest that the mediodorsal (MD) thalamus links primary olfactory (piriform) cortex to olfactory neocortical projection sites in orbitofrontal cortex (OFC), this transthalamic route is regarded to be inconsequential, particularly compared with a direct monosynaptic pathway linking piriform cortex and OFC. In this study, we combined functional magnetic resonance imaging with novel effective connectivity techniques to measure attention-dependent network coherence within direct (nonthalamic) and indirect (transthalamic) olfactory pathways. Human subjects were presented with (or without) an odor and with (or without) a tone, while selectively attending to either modality. Attention to odor significantly modulated neural coupling within the indirect pathway, strengthening MD thalamus-OFC connectivity. Critically, these effects were modality specific (odor > tone attention), directionally sensitive (forward > backward connections), and selective to route (indirect > direct pathway). Our findings support the idea that the human transthalamic pathway is an active modulatory target of olfactory attention. The results imply that olfaction, like all other sensory modalities, requires a thalamic relay, if only to consciously analyze a smell.

The feeling of familiarity of music and odors: the same neural signature?

The feeling of familiarity can be triggered by stimuli from all sensory modalities, suggesting a multimodal nature of its neural bases. In the present experiment, we investigated this hypothesis by studying the neural bases of familiarity processing of odors and music. In particular, we focused on familiarity referring to the participants' life experience. Items were classified as familiar or unfamiliar based on participants' individual responses, and activation patterns evoked by familiar items were compared with those evoked by unfamiliar items. For the feeling of familiarity, a bimodal activation pattern was observed in the left hemisphere, specifically the superior and inferior frontal gyri, the precuneus, the angular gyrus, the parahippocampal gyrus, and the hippocampus. Together with previously reported data on verbal items, visual items, and auditory items other than music, this outcome suggests a multimodal neural system of the feeling of familiarity. The feeling of unfamiliarity was related to a smaller bimodal activation pattern mainly located in the right insula and likely related to the detection of novelty.

Involvement of the left anterior insula and frontopolar gyrus in odor discrimination.

Discriminating between successively presented odors requires brief storage of the first odor's perceptual trace, which then needs to be subsequently compared to the second odor in the pair. This study explores the cortical areas involved in odor discrimination and compares them with findings from studies of working-memory, traditionally investigated with n-back paradigms. Sixteen right-handed subjects underwent H(2) (15)O positron emission tomography during counterbalanced conditions of odorless sniffing, repeated single odor detection, multiple odor detection, and conscious successive discrimination between odor pairs. Eight odorants were delivered using a computer-controlled olfactometer through a birhinal nasal cannula. Conscious successive odor discrimination evoked significantly greater activity in the left anterior insula and frontopolar gyrus when compared to reported sensory detection of the identical odors. Additional activation was found in the left lateral orbital/inferior frontal and middle frontal gyri when discrimination was compared to the odorless condition. The left anterior insula is likely involved in the evaluation of odor properties. Consistent with other studies, frontopolar and middle frontal gyrus activation is more likely related to working memory during odor discrimination.

Left temporo-limbic and orbital dysfunction in schizophrenia during odor familiarity and hedonicity judgments.

Impairments of olfactory processing in patients with schizophrenia (SZ) have been reported in various olfactory tasks such as detection, discrimination, recognition memory, identification, and naming. The purpose of our study was to determine whether impairments in odor familiarity and hedonicity judgments observed in SZ patients during a previous behavioral study are associated with modifications of the activation patterns in olfactory areas. Twelve SZ patients, and 12 healthy comparison (HC) subjects, were tested using the H2(15)O-PET technique and 48 different odorants delivered during 8 scans. In addition to an odorless baseline condition, they had either to detect odor, or to judge odor familiarity or hedonicity, giving their responses by pressing a button. Regional cerebral blood flows during olfactory conditions were compared with those for baseline condition. Between-group analyses were then performed, and completed by regions of interest analyses. Both groups had equivalent ability for the detection of suprathreshold odorants, but patients found odors less familiar, and pleasant odors less pleasant than HC subjects. These behavioral results were related to functional abnormalities in temporo-limbic and orbital olfactory regions lateralized in the left hemisphere: the posterior part of the piriform cortex and orbital regions for familiarity judgments, the insular gyrus for hedonicity judgments, and the left inferior frontal gyrus and anterior piriform cortex/putamen region for the three olfactory tasks. They mainly resulted from a lack of activation during task conditions in the SZ patients. These data could explain olfactory disturbances and other clinical features of schizophrenia such as anhedonia.