High-resolution fMRI Reveals Match Enhancement and Attentional Modulation in the Human Medial Temporal Lobe

A primary function of the medial temporal lobe (MTL) is to signal prior encounter with behaviorally relevant stimuli. MTL match enhancement—increased activation when viewing previously encountered stimuli—has been observed for goal-relevant stimuli in nonhuman primates during delayed-match-to-sample tasks and in humans during more complex relational memory tasks. Match enhancement may alternatively reflect (a) an attentional response to familiar relative to novel stimuli or (b) the retrieval of contextual details surrounding the past encounter with familiar stimuli. To gain leverage on the functional significance of match enhancement in the hippocampus, high-resolution fMRI of human MTL was conducted while participants attended, ignored, or passively viewed face and scene stimuli in the context of a modified delayed-match-to-sample task. On each “attended” trial, two goal-relevant stimuli were encountered before a probe that either matched or mismatched one of the attended stimuli, enabling examination of the consequences of encountering one of the goal-relevant stimuli as a match probe on later memory for the other (nonprobed) goal-relevant stimulus. fMRI revealed that the hippocampus was insensitive to the attentional manipulation, whereas parahippocampal cortex was modulated by scene-directed attention, and perirhinal cortex showed more subtle and general effects of attention. By contrast, all hippocampal subfields demonstrated match enhancement to the probe, and a postscan test revealed more accurate recognition memory for the nonprobed goal-relevant stimulus on match relative to mismatch trials. These data suggest that match enhancement in human hippocampus reflects retrieval of other goal-relevant contextual details surrounding a stimulus's prior encounter.

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High-resolution fMRI of Content-sensitive Subsequent Memory Responses in Human Medial Temporal Lobe

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2009.21195 ◽

2010 ◽

Vol 22 (1) ◽

pp. 156-173 ◽

Cited By ~ 78

Author(s):

Alison R. Preston ◽

Aaron M. Bornstein ◽

J. Benjamin Hutchinson ◽

Meghan E. Gaare ◽

Gary H. Glover ◽

...

Keyword(s):

High Resolution ◽

Dentate Gyrus ◽

Temporal Lobe ◽

Medial Temporal Lobe ◽

Functional Neuroimaging ◽

Perirhinal Cortex ◽

Memory Effects ◽

Long Term Memory ◽

Memory Strength ◽

Parahippocampal Cortex

The essential role of the medial temporal lobe (MTL) in long-term memory for individual events is well established, yet important questions remain regarding the mnemonic functions of the component structures that constitute the region. Within the hippocampus, recent functional neuroimaging findings suggest that formation of new memories depends on the dentate gyrus and the CA3 field, whereas the contribution of the subiculum may be limited to retrieval. During encoding, it has been further hypothesized that structures within MTL cortex contribute to encoding in a content-sensitive manner, whereas hippocampal structures may contribute to encoding in a more domain-general manner. In the current experiment, high-resolution fMRI techniques were utilized to assess novelty and subsequent memory effects in MTL subregions for two classes of stimuli—faces and scenes. During scanning, participants performed an incidental encoding (target detection) task with novel and repeated faces and scenes. Subsequent recognition memory was indexed for the novel stimuli encountered during scanning. Analyses revealed voxels sensitive to both novel faces and novel scenes in all MTL regions. However, similar percentages of voxels were sensitive to novel faces and scenes in perirhinal cortex, entorhinal cortex, and a combined region comprising the dentate gyrus, CA2, and CA3, whereas parahippocampal cortex, CA1, and subiculum demonstrated greater sensitivity to novel scene stimuli. Paralleling these findings, subsequent memory effects in perirhinal cortex were observed for both faces and scenes, with the magnitude of encoding activation being related to later memory strength, as indexed by a graded response tracking recognition confidence, whereas subsequent memory effects were scene-selective in parahippocampal cortex. Within the hippocampus, encoding activation in the subiculum correlated with subsequent memory for both stimulus classes, with the magnitude of encoding activation varying in a graded manner with later memory strength. Collectively, these findings suggest a gradient of content sensitivity from posterior (parahippocampal) to anterior (perirhinal) MTL cortex, with MTL cortical regions differentially contributing to successful encoding based on event content. In contrast to recent suggestions, the present data further indicate that the subiculum may contribute to successful encoding irrespective of event content.

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Children show adult-like hippocampal pattern separation for familiar but not novel events

10.31234/osf.io/3d8tv ◽

2020 ◽

Author(s):

Susan L. Benear ◽

Elizabeth A. Horwath ◽

Emily Cowan ◽

M. Catalina Camacho ◽

Chi Ngo ◽

...

Keyword(s):

Episodic Memory ◽

Temporal Lobe ◽

Medial Temporal Lobe ◽

Developmental Change ◽

Pattern Separation ◽

Developmental Changes ◽

Similarity Analysis ◽

Separation Processes ◽

Parahippocampal Cortex ◽

Pattern Similarity

The medial temporal lobe (MTL) undergoes critical developmental change throughout childhood, which aligns with developmental changes in episodic memory. We used representational similarity analysis to compare neural pattern similarity for children and adults in hippocampus and parahippocampal cortex during naturalistic viewing of clips from the same movie or different movies. Some movies were more familiar to participants than others. Neural pattern similarity was generally lower for clips from the same movie, indicating that related content taxes pattern separation-like processes. However, children showed this effect only for movies with which they were familiar, whereas adults showed the effect consistently. These data suggest that children need more exposures to stimuli in order to show mature pattern separation processes.

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Differences in Mnemonic Processing by Neurons in the Human Hippocampus and Parahippocampal Regions

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2006.18.10.1654 ◽

2006 ◽

Vol 18 (10) ◽

pp. 1654-1662 ◽

Cited By ~ 77

Author(s):

Indre V. Viskontas ◽

Barbara J. Knowlton ◽

Peter N. Steinmetz ◽

Itzhak Fried

Keyword(s):

Recognition Memory ◽

Temporal Lobe ◽

Medial Temporal Lobe ◽

Computational Models ◽

Systems Approach ◽

Declarative Memory ◽

Neuronal Firing ◽

Psychological Review ◽

Firing Patterns ◽

Human Hippocampus

Different structures within the medial-temporal lobe likely make distinct contributions to declarative memory. In particular, several current psychological and computational models of memory predict that the hippocampus and parahippocampal regions play different roles in the formation and retrieval of declarative memories [e.g., Norman, K. A., & O'Reilly, R. C. Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning systems approach. Psychological Review, 110, 611–646, 2003]. Here, we examined the neuronal firing patterns in these two regions during recognition memory. Recording directly from neurons in humans, we find that cells in both regions respond to novel stimuli with an increase in firing (excitation). However, already on the second presentation of a stimulus, neurons in these regions show very different firing patterns. In the parahippocampal region there is dramatic decrease in the number of cells responding to the stimuli, whereas in the hippocampus there is recruitment of a large subset of neurons showing inhibitory (decrease from baseline firing) responses. These results suggest that inhibition is a mechanism used by cells in the human hippocampus to support sparse coding in mnemonic processing. The findings also provide further evidence for the division of labor in the medial-temporal lobe with respect to declarative memory processes.

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Volumetric GWAS of medial temporal lobe structures identifies an ERC1 locus using ADNI high-resolution T2-weighted MRI data

Neurobiology of Aging ◽

10.1016/j.neurobiolaging.2020.07.005 ◽

2020 ◽

Vol 95 ◽

pp. 81-93

Author(s):

Shan Cong ◽

Xiaohui Yao ◽

Zhi Huang ◽

Shannon L. Risacher ◽

Kwangsik Nho ◽

...

Keyword(s):

High Resolution ◽

Temporal Lobe ◽

Medial Temporal Lobe

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Forward Processing of Object–Location Association from the Ventral Stream to Medial Temporal Lobe in Nonhuman Primates

Cerebral Cortex ◽

10.1093/cercor/bhz164 ◽

2019 ◽

Vol 30 (3) ◽

pp. 1260-1271 ◽

Cited By ~ 5

Author(s):

He Chen ◽

Yuji Naya

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Spatial Information ◽

Object Location ◽

Object Identity ◽

Downstream Target ◽

Parahippocampal Cortex ◽

Ventral Pathway ◽

Additive Form ◽

Location Association

Abstract While the hippocampus (HPC) is a prime candidate combining object identity and location due to its strong connections to the ventral and dorsal pathways via surrounding medial temporal lobe (MTL) areas, recent physiological studies have reported spatial information in the ventral pathway and its downstream target in MTL. However, it remains unknown whether the object–location association proceeds along the ventral MTL pathway before HPC. To address this question, we recorded neuronal activity from MTL and area anterior inferotemporal cortex (TE) of two macaques gazing at an object to retain its identity and location in each trial. The results showed significant effects of object–location association at a single-unit level in TE, perirhinal cortex (PRC), and HPC, but not in the parahippocampal cortex. Notably, a clear area difference emerged in the association form: 1) representations of object identity were added to those of subjects’ viewing location in TE; 2) PRC signaled both the additive form and the conjunction of the two inputs; and 3) HPC signaled only the conjunction signal. These results suggest that the object and location signals are combined stepwise at TE and PRC each time primates view an object, and PRC may provide HPC with the conjunctional signal, which might be used for encoding episodic memory.

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Alternate Task Inhibits Single-neuron Category-selective Responses in the Human Hippocampus while Preserving Selectivity in the Amygdala

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2008.21017 ◽

2009 ◽

Vol 21 (2) ◽

pp. 347-358 ◽

Cited By ~ 7

Author(s):

Peter N. Steinmetz

Keyword(s):

Temporal Lobe ◽

Video Game ◽

Medial Temporal Lobe ◽

Hippocampal Neurons ◽

Single Neuron ◽

Single Neurons ◽

Human Epilepsy ◽

Human Hippocampus ◽

The Subject

One fifth of neurons in the medial-temporal lobe of human epilepsy patients respond selectively to categories of images, such as faces or cars. Here we show that responses of hippocampal neurons are rapidly modified as subjects alternate (over 60 sec) between two tasks (1) identifying images from a category, or (2) playing a simple video game superimposed on the same images. Category-selective responses, present when a subject identifies categories, are eliminated when the subject shifts to playing the game for 87% of category-selective hippocampal neurons. By contrast, responses in the amygdala are present during both tasks for 72% of category-selective amygdalar neurons. These results suggest that attention to images is required to evoke selective responses from single neurons in the hippocampus, but is not required by neurons in the amygdala.

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High-resolution fMRI investigation of the medial temporal lobe

Human Brain Mapping ◽

10.1002/hbm.20331 ◽

2007 ◽

Vol 28 (10) ◽

pp. 959-966 ◽

Cited By ~ 77

Author(s):

C. Brock Kirwan ◽

Craig K. Jones ◽

Michael I. Miller ◽

Craig E.L. Stark

Keyword(s):

High Resolution ◽

Temporal Lobe ◽

Medial Temporal Lobe

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Representations of local spatial information in the human medial temporal lobe during memory-guided navigation

10.1101/2020.11.18.389346 ◽

2020 ◽

Author(s):

Shao-Fang Wang ◽

Valerie A. Carr ◽

Serra E. Favila ◽

Jeremy N. Bailenson ◽

Thackery I. Brown ◽

...

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Spatial Information ◽

Activity Patterns ◽

Critical Role ◽

Neural Representations ◽

Parahippocampal Cortex ◽

Pattern Similarity ◽

Cortical Regions ◽

Goal Directed Behavior

AbstractThe 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.

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