publications

preprints

1. Representations of local spatial information in the human medial temporal lobe during memory-guided navigation Wang S-F, Carr VA, Favila SE, Bailenson JN, Brown TI, Jiang J, & Wagner AD bioRxiv (2020) [Abstract] [HTML] [PDF]

   The hippocampus (HC) and surrounding medial temporal lobe (MTL) cortical regions play a critical role in spatial navigation and episodic memory. However, it remains unclear how the interaction between the HC’s conjunctive coding and mnemonic differentiation contributes to neural representations of spatial environments. Multivariate functional magnetic resonance imaging (fMRI) analyses enable examination of how human HC and MTL cortical regions encode multidimensional spatial information to support memory-guided navigation. We combined high-resolution fMRI with a virtual navigation paradigm in which participants relied on memory of the environment to navigate to goal locations in two different virtual rooms. Within each room, participants were cued to navigate to four learned locations, each associated with one of two reward values. Pattern similarity analysis revealed that when participants successfully arrived at goal locations, activity patterns in HC and parahippocampal cortex (PHC) represented room-goal location conjunctions and activity patterns in HC subfields represented room-reward-location conjunctions. These results add to an emerging literature revealing hippocampal conjunctive representations during goal-directed behavior.

peer-reviewed

1. Perception and memory have distinct spatial tuning properties in human visual cortex Favila SE, Kuhl BA, & Winawer J Nature Communications (2022) [Abstract] [HTML] [PDF] [Data] [Media Coverage]

   Reactivation of earlier perceptual activity is thought to underlie long-term memory recall. Despite evidence for this view, it is unclear whether mnemonic activity exhibits the same tuning properties as feedforward perceptual activity. Here, we leverage population receptive field models to parameterize fMRI activity in human visual cortex during spatial memory retrieval. Though retinotopic organization is present during both perception and memory, large systematic differences in tuning are also evident. Whereas there is a three-fold decline in spatial precision from early to late visual areas during perception, this pattern is not observed during memory retrieval. This difference cannot be explained by reduced signal-to-noise or poor performance on memory trials. Instead, by simulating top-down activity in a network model of cortex, we demonstrate that this property is well explained by the hierarchical structure of the visual system. Together, modeling and empirical results suggest that computational constraints imposed by visual system architecture limit the fidelity of memory reactivation in sensory cortex.

2. Abrupt hippocampal remapping signals resolution of memory interference Wanjia G, Favila SE, Kim G, Molitor RJ, & Kuhl BA Nature Communications (2021) [Abstract] [HTML] [PDF] [Data]

   Remapping refers to a decorrelation of hippocampal representations of similar spatial environments. While it has been speculated that remapping may contribute to the resolution of episodic memory interference in humans, direct evidence is surprisingly limited. We tested this idea using high-resolution, pattern-based fMRI analyses. Here we show that activity patterns in human CA3/dentate gyrus exhibit an abrupt, temporally-specific decorrelation of highly similar memory representations that is precisely coupled with behavioral expressions of successful learning. The magnitude of this learning-related decorrelation was predicted by the amount of pattern overlap during initial stages of learning, with greater initial overlap leading to stronger decorrelation. Finally, we show that remapped activity patterns carry relatively more information about learned episodic associations compared to competing associations, further validating the learning-related significance of remapping. Collectively, these findings establish a critical link between hippocampal remapping and episodic memory interference and provide insight into why remapping occurs.

3. Transforming the concept of memory reactivation Favila SE, Lee H, & Kuhl BA Trends in Neurosciences (2020) [Abstract] [HTML] [PDF]

   Reactivation refers to the phenomenon wherein patterns of neural activity expressed during perceptual experience are re-expressed at a later time, a putative neural marker of memory. Reactivation of perceptual content has been observed across many cortical areas and correlates with objective and subjective expressions of memory in humans. However, because reactivation emphasizes similarities between perceptual and memory-based representations, it obscures differences in how perceptual events and memories are represented. Here, we highlight recent evidence of systematic differences in how (and where) perceptual events and memories are represented in the brain. We argue that neural representations of memories are best thought of as spatially transformed versions of perceptual representations. We consider why spatial transformations occur and identify critical questions for future research.

4. Parietal representations of stimulus features are amplified during memory retrieval and flexibly aligned with top-down goals Favila SE, Samide R, Sweigart SC, & Kuhl BA Journal of Neuroscience (2018) [Abstract] [HTML] [PDF]

   In studies of human episodic memory, the phenomenon of reactivation has traditionally been observed in regions of occipitotemporal cortex (OTC) involved in visual perception. However, reactivation also occurs in lateral parietal cortex (LPC), and recent evidence suggests that stimulus-specific reactivation may be stronger in LPC than in OTC. These observations raise important questions about the nature of memory representations in LPC and their relationship to representations in OTC. Here, we report two fMRI experiments that quantified stimulus feature information (color and object category) within LPC and OTC, separately during perception and memory retrieval, in male and female human subjects. Across both experiments, we observed a clear dissociation between OTC and LPC: while feature information in OTC was relatively stronger during perception than memory, feature information in LPC was relatively stronger during memory than perception. Thus, while OTC and LPC represented common stimulus features in our experiments, they preferentially represented this information during different stages. In LPC, this bias toward mnemonic information co-occurred with stimulus-level reinstatement during memory retrieval. In Experiment 2, we considered whether mnemonic feature information in LPC was flexibly and dynamically shaped by top-down retrieval goals. Indeed, we found that dorsal LPC preferentially represented retrieved feature information that addressed the current goal. In contrast, ventral LPC represented retrieved features independent of the current goal. Collectively, these findings provide insight into the nature and significance of mnemonic representations in LPC and constitute an important bridge between putative mnemonic and control functions of parietal cortex.

5. Individual differences in associative memory among older adults explained by hippocampal subfield structure and function Carr VA, Bernstein JD, Favila SE, Rutt BK, Kerchner GA, & Wagner AD Proceedings of the National Academy of Sciences (2017) [Abstract] [HTML] [PDF] [Data]

   Older adults differ in the degree to which they experience memory impairments, but the underlying factors contributing to this variability remain unclear. Motivated by the essential role of the medial temporal lobe (MTL) in declarative memory, we investigated whether episodic memory differences among older adults can be explained by differences in MTL subfield structure and function. Using high-resolution magnetic resonance imaging, we demonstrated that a combination of structural and functional subfield measures significantly accounted for differences in memory performance. These findings advance understanding of how independent but converging influences of both MTL structure and function contribute to age-related impairment in episodic memory, complementing findings in the rodent and human postmortem literatures.

6. Overlap among spatial memories triggers repulsion of hippocampal representations Chanales AJH, Oza A, Favila SE, & Kuhl BA Current Biology (2017) [Abstract] [HTML] [PDF] [Data]

   Across the domains of spatial navigation and episodic memory, the hippocampus is thought to play a critical role in disambiguating (pattern separating) representations of overlapping events. However, it is not fully understood how and why hippocampal patterns become separated. Here, we test the idea that event overlap triggers a “repulsion” among hippocampal representations that develops over the course of learning. Using a naturalistic route-learning paradigm and spatiotemporal pattern analysis of human fMRI data, we found that hippocampal representations of overlapping routes gradually diverged with learning to the point that they became less similar than representations of non-overlapping events. In other words, the hippocampus not only disambiguated overlapping events but formed representations that “reversed” the objective similarity among routes. This finding, which was selective to the hippocampus, is not predicted by standard theoretical accounts of pattern separation. Critically, because the overlapping route stimuli that we used ultimately diverged (so that each route contained overlapping and non-overlapping segments), we were able to test whether the reversal effect was selective to the overlapping segments. Indeed, once overlapping routes diverged (eliminating spatial and visual similarity), hippocampal representations paradoxically became relatively more similar. Finally, using a novel analysis approach, we show that the degree to which individual hippocampal voxels were initially shared across route representations was predictive of the magnitude of learning-related separation. Collectively, these findings indicate that event overlap triggers a repulsion of hippocampal representations—a finding that provides critical mechanistic insight into how and why hippocampal representations become separated.

7. Prospective representation of navigational goals in the human hippocampus Brown TI, Carr VA, LaRocque KF, Favila SE, Gordon AM, Bowles B, Bailenson JN, & Wagner AD Science (2016) [Abstract] [HTML] [PDF]

   Mental representation of the future is a fundamental component of goal-directed behavior. Computational and animal models highlight prospective spatial coding in the hippocampus, mediated by interactions with the prefrontal cortex, as a putative mechanism for simulating future events. Using whole-brain high-resolution functional magnetic resonance imaging and multi-voxel pattern classification, we tested whether the human hippocampus and interrelated cortical structures support prospective representation of navigational goals. Results demonstrated that hippocampal activity patterns code for future goals to which participants subsequently navigate, as well as for intervening locations along the route, consistent with trajectory-specific simulation. The strength of hippocampal goal representations covaried with goal-related coding in the prefrontal, medial temporal, and medial parietal cortex. Collectively, these data indicate that a hippocampal-cortical network supports prospective simulation of navigational events during goal-directed planning.

8. Experience-dependent hippocampal pattern differentiation prevents interference during subsequent learning Favila SE, Chanales AJH, & Kuhl BA Nature Communications (2016) [Abstract] [HTML] [PDF]

   The hippocampus is believed to reduce memory interference by disambiguating neural representations of similar events. However, there is limited empirical evidence linking representational overlap in the hippocampus to memory interference. Likewise, it is not fully understood how learning influences overlap among hippocampal representations. Using pattern-based fMRI analyses, we tested for a bidirectional relationship between memory overlap in the human hippocampus and learning. First, we show that learning drives hippocampal representations of similar events apart from one another. These changes are not explained by task demands to discriminate similar stimuli and are fully absent in visual cortical areas that feed into the hippocampus. Second, we show that lower representational overlap in the hippocampus benefits subsequent learning by preventing interference between similar memories. These findings reveal targeted experience-dependent changes in hippocampal representations of similar events and provide a critical link between memory overlap in the hippocampus and behavioural expressions of memory interference.

9. Stimulating memory consolidation Favila SE & Kuhl BA Nature Neuroscience (News and Views) (2014) [Abstract] [HTML] [PDF]

   A study in this issue of Nature Neuroscience reports that administering caffeine to humans immediately after memory encoding enhances consolidation, as reflected by improved performance in a memory test a day later.