The Neural Foundations for Memory and Social Cognition in the Human Brain

National Institute Of Mental Health

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Abstract

During this past year we have concentrated our efforts on addressing outstanding issues concerning three major divisions of memory: semantic memory composed of our knowledge about things and ideas, autobiographical memory composed of our recollections of life events, and priming, a form of implicit memory that underlies our ability to recognize objects and words fast and efficiently. Several of our studies of semantic memory have focused on the relationship between the neural systems for representing higher-order conceptual information and lower-level sensory information. We recently established that taste information (sweet, salty, and sour tastes) is represented in gustatory cortex by a population code, rather than by a taste-specific spatial map (Avery et al., Journal of Neuroscience, 2020). Building on this finding we asked whether simply viewing pictures of foods defined primarily by their dominant taste (e.g., pictures of candy, pretzels, lemons) would activate the same region of gustatory cortex active when experiencing these tastes, and whether these 'inferred tastes' were also represented by a population code. We found that this was indeed the case. Viewing food pictures triggered the automatic retrieval of specific taste quality information associated with the depicted foods and that this information was represented by a population code (Avery et al., Proceedings of the National Academy of Sciences, 2021). These results also showed how higher-order inferences derived from stimuli in one modality (i.e., vision) can be represented in a region of the brain typically thought to represent only low-level information about a different modality (i.e., taste). On the behavioral level, we have been interested in understanding why the words we use to label tastes are often used metaphorically to describe emotional experiences (e.g., Parting is such sweet sorrow, right to the bitter end). Clearly, taste metaphors provide a rich vocabulary for describing emotional experience, perhaps by serving as an adaptive mechanism for conveying abstract emotional concepts using concrete verbal references to our shared experience. We hypothesized that the popularity of these expressions results from the close association with hedonic valence shared by these two domains of experience. To explore the possibility that this affective quality underlies the semantic similarity of these domains, we used a behavioral odd-one-out task in an online sample of 1059 participants in order to examine the semantic similarity of concepts related to emotion, taste, and color, another rich source of sensory metaphors. We found that the semantic similarity of emotion and taste concepts was greater than that of emotion and color concepts. Importantly, the similarity of taste and emotion concepts was strongly related to their similarity in hedonic valence, a relationship which was also significantly greater than between color and emotion. These results suggest that the common core of valence between taste and emotion concepts allows us to bridge the conceptual divide between our shared sensory environment and our internal emotional experience (Avery et al., Frontiers in Psychology, 2022). We are also interested in how memory for our life events (autobiographical memory) are represented in the brain. For several decades, the role played by the hippocampus (a major brain region in memory functioning) in retrieving autobiographical memories has been hotly debated. One model (The Standard Consolidation Model) asserts that via a time-dependent process of cortical consolidation, the hippocampus is no longer required for successful retrieval of remote events (e.g., childhood memories). In contrast, others have argued that the critical determinate of hippocampal involvement is not how long ago the event occurred, but the precision and detail of the memory. In this view, the hippocampus is always required for vividly recalling memories (The Multiple Trace hypothesis). The debate for and against temporally graded activity in the hippocampus rests largely on the subjective phenomenology of retrieved memories. In this regard, fMRI studies of autobiographical memory have suffered due to their reliance upon covert, or silent, recall because of concerns about in-scanner head motion. We overcame this problem by capitalizing on recent advances in fMRI acquisition and analysis that allowed our participants to overtly recall aloud their recent and remote memories during scanning. In accordance with the predictions of the Standard Consolidation Model, we found that the hippocampus became less and less active the more remote the retrieved memory, with no hippocampal activity detected for memories recalled from the most distant past. Moreover, by careful analysis of the actual verbal memory reports generated by our participants, we were able to show that this result was not due to the amount or quality of the details recalled (Gilmore et al., Proceedings of the National Academy, 2021). Interestingly, the above findings held only for the more posterior region of the hippocampus. The anterior regions failed to show any evidence of activity during autobiographical memory recall at any timepoint. Recent evidence suggests, however, that the anterior and posterior hippocampus make distinct functional contributions to memory retrieval. Specifically, recall is characterized by an early stage of memory construction and a later stage of detailed elaboration, which may engage different regions of the hippocampus. To evaluate this possibility, we focused on the early stage of retrieval where participants searched for and selected a memory for later elaboration. We now found no evidence of a temporal gradient during this memory construction stage, instead observing strong anterior hippocampus activity regardless of memory remoteness. These findings suggest a unique contribution of the anterior hippocampus to the construction process of autobiographical retrieval. Taken together with our previous findings on the posterior region of the hippocampus, these findings highlight that retrieval processes, which have yet to be integrated with current models of systems consolidation, offer novel insights into hippocampal subregion function over time (Audrain et al., Journal of Neuroscience, 2022). Finally, our studies of implicit memory have focused on the behavioral and neural underpinnings of a powerful form of learning known as priming. It has longed been recognized that our ability to identify a stimulus improves with repetition (repetition priming), whereas neural activity decreases (repetition suppression) (Gotts et al., Communications Biology, 2021). In our most recent study on this topic, we evaluated the effects of lesions to different parts of the cerebral cortex (both from stroke and surgical intervention for the relief of intractable epilepsy) on relatively short (30 minute) and long (three month) delays between repetitions of objects. Overall, patients exhibited significant repetition priming at both short and long delays. However, patients with frontal resections (largely anterior and medially) differed significantly from those with right anterior temporal resections in showing fully intact short-term priming but absent long-term priming. In contrast, patients with left lateral frontal damage exhibited impaired short-term priming relative to other frontal damage locations, These findings suggest that the lateral and anteromedial regions of frontal cortex play distinct roles in mediating repetition priming at short-lag and long-lag timescales, respectively (Milleville et al., Neuropsychologia, 2022).