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

National Institute Of Mental Health

Investigators

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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, located in a region of the brain known as the insula, by a population code, rather than by a taste-specific spatial map (Avery et al., Journal of Neuroscience, 2020). We also found that simply viewing pictures of different types of foods (e.g., candy, pretzels, lemons) triggered the automatic retrieval of specific taste quality information associated with the depicted foods (sweet, salty, and sour) and that this information was also represented by a population code in the same region of the insula where the experience of taste is represented (Avery et al., Proceedings of the National Academy of Sciences, 2021). Most recently, we have now found that the same finding holds when subjects are asked to simply imagine specific tastes (sweet, salty, and sour) (Avery et al., Progress in Neurobiology, 2023). These results reveal how information about a critical property of food (taste) is represented in the brain. They also show how higher-order inferences derived from visual perception and imagination can be represented in a region of the brain typically thought to represent only low-level sensory information (i.e., taste), thus adding new insights into multimodal nature of cortical processing (Martin, Language, Cognition, and Neuroscience, 2023). We are also interested in how memory for our life events (autobiographical memory) is represented in the brain. Previous neural imaging studies of autobiographical memory have produced conflicting results largely due to 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 (Gilmore et al., Frontiers in Neuroscience, 2022). Using these methodological advances 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 (Gilmore et al., Proceedings of the National Academy of Sciences, 2021). However, this finding held only for the more posterior regions of the hippocampus. The anterior regions failed to show any evidence of activity during 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 when participants searched for and selected a memory for later elaboration. We now found strong activation of the more anterior regions of the hippocampus. Moreover, this activity was constant regardless of the remoteness of the memory that was retrieved. 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 memory consolidation, offer novel insights into hippocampal subregion function over time (Audrain et al., Journal of Neuroscience, 2022; Gilmore et al., Cognitive 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 a 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 (mostly of the anteriomedial regions) showed intact short-term, but not long-term priming. In contrast, patients with left lateral frontal damage exhibited impaired short-term priming. 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). We are now pursuing this issue in typically developing individuals using simultaneous recording of both electroencephalic (EEG) and fMRI data. This approach, by providing markedly increased temporal and spatial resolution, should provide unique insights into the neural mechanism underpinning this basic form of learning.