Involvement of hippocampal subfields and anterior-posterior subregions in encoding and retrieval of item, spatial, and associative memories: Longitudinal versus transverse axis

Hrybouski, Stanislau; MacGillivray, Melanie; Huang, Yushan; Madan, Christopher R.; Carter, Rawle; Seres, Peter; Malykhin, Nikolai

doi:10.1016/j.neuroimage.2019.01.061

Cited by 45 publications

(51 citation statements)

References 174 publications

(332 reference statements)

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“…Of note, in spite of the lower spatial resolution (1.7 mm 3 ) used here, our step function clusters appear to primarily overlap with DG/CA3 (Figure 2). These relatively more posterior clusters are also consistent with the notion that posterior hippocampus is involved in detailed episodic memories (Hrybouski et al, 2019;Poppenk, Evensmoen, Moscovitch, & Nadel, 2013;Strange, Witter, Lein, & Moser, 2014), which is necessary for successful MD.…”

Section: Discussionsupporting

confidence: 85%

“…For the hippocampus, we reported the location of significant clusters by delineating hippocampal head, body, and tail at y = −20 and −35 in MNI space, in line with prior work (DeMaster & Ghetti, ; Sastre, Wendelken, Lee, Bunge, & Ghetti, ), to inform literature suggesting functional specialization along the longitudinal axis of the hippocampus (Hrybouski et al, ). We also overlaid significant clusters on a standard hippocampal subfield template (Stark & Stark, ).…”

Section: Methodssupporting

confidence: 80%

“…A higher-level analysis then assessed the mean of this step function across the group using one EV to model each participant's mean step function from the mid-level analysis and a bidirectional (two-tailed) contrast to assess the step function as above. (Hrybouski et al, 2019). We also overlaid significant clusters on a standard hippocampal subfield template .…”

Section: Analysesmentioning

confidence: 99%

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Neural substrates of mnemonic discrimination: A whole‐brain fMRI investigation

2020

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Introduction A fundamental component of episodic memory is the ability to differentiate new and highly similar events from previously encountered events. Numerous functional magnetic resonance imaging (fMRI) studies have identified hippocampal involvement in this type of mnemonic discrimination (MD), but few studies have assessed MD‐related activity in regions beyond the hippocampus. Therefore, the current fMRI study examined whole‐brain activity in healthy young adults during successful discrimination of the test phase of the Mnemonic Similarity Task. Method In the study phase, participants made “indoor”/“outdoor” judgments to a series of objects. In the test phase, they made “old”/“new” judgments to a series of probe objects that were either repetitions from the memory set (targets), similar to objects in the memory set (lures), or novel. We assessed hippocampal and whole‐brain activity consistent with MD using a step function to identify where activity to targets differed from activity to lures with varying degrees of similarity to targets (high, low), responding to them as if they were novel. Results Results revealed that the hippocampus and occipital cortex exhibited differential activity to repeated stimuli relative to even highly similar stimuli, but only hippocampal activity predicted discrimination performance. Conclusions These findings are consistent with the notion that successful MD is supported by the hippocampus, with auxiliary processes supported by cortex (e.g., perceptual discrimination).

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Section: Discussionsupporting

confidence: 85%

Section: Methodssupporting

confidence: 80%

Section: Analysesmentioning

confidence: 99%

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Neural substrates of mnemonic discrimination: A whole‐brain fMRI investigation

2020

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“…Studies with high-resolution fMRI scans may be able to provide a better understanding of the developmental effects in the hippocampus in the future. Recent continued interest has started to quantify the difference in the long-axis functional connectivity with special consideration of the subregions and encoding/retrieval dynamics (e.g., Hrybouski et al, 2019). Using ultra-high resolution structural MRI and high-resolution fMRI measures, they identified an anterior-posterior gradient in hippocampal activity when comparing encoding and retrieval.…”

Section: Discussionmentioning

confidence: 99%

Differential Functional Connectivity in Anterior and Posterior Hippocampus Supporting the Development of Memory Formation

Tang

Pruitt

et al. 2020

Front. Hum. Neurosci.

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Neuroimaging evidence suggests that the development of the hippocampus, a brain structure critical for memory function, contributes to the improvements of episodic memory between middle childhood to adulthood. However, investigations on age differences in hippocampal activation and functional connectivity and their contributions to the development of memory have yielded mixed results. Given the known structural and functional heterogeneity along the long axis of the hippocampus, we investigated age differences in the activation and functional connectivity in hippocampal subregions with a cross-sectional sample of 96 participants ages 8-25 years. We found that anterior and posterior hippocampus supported memory formation, and there was overall stability in memory-related hippocampal activation with age. Without taking account of memory outcome, direct contrast between subregions showed higher functional connectivity of anterior, compared to the posterior hippocampus, with regions in the inferior frontal and lateral temporal lobes, and higher functional connectivity of posterior, compared to the anterior hippocampus, with regions in the medial and superior frontal, inferior parietal, and occipital lobes. A direct contrast between the memory-related connectivity patterns of anterior and posterior hippocampus identified a region in the medial frontal cortex, with which anterior and posterior hippocampus was differentially functionally connected. Finally, we identified age differences in memory-related differential hippocampal functional connectivity with several frontal and visual/sensory cortices, underscoring the importance of examining age differences in the patterns of hippocampal connectivity. Moreover, the specific patterns of differential anterior and posterior functional connectivity indicate an increase in the functional specialization along the long axis of the hippocampus and a dynamic shift in hippocampal connectivity patterns that supports memory development.

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“…Responses within the AH were heterogenous: reinforcement encoding was strongest in the anterior body whereas the online goal cell-like responses were strongest in the head. This heterogeneity may not be a function of long axis location per se but simply reflect the folding of human AH, with the anterior-most portion of the head being comprised mostly of CA3/CA1 and lacking the dentate gyrus (DG; Hrybouski et al, 2019). Thus, the goal-cell like responses in the hippocampal head likely originate in the CA3/CA1 or the subiculum and not in the DG.…”

Section: Discussionmentioning

confidence: 99%

Differential reinforcement encoding along the hippocampal long axis helps resolve the explore/exploit dilemma

Dombrovski

Luna

Hallquist

2020

Preprint

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Hippocampal maps incorporate reward information, yet the functional contributions of the anterior and posterior hippocampal divisions (AH and PH) to reinforcement learning remain unclear. Here, we examined exploration and exploitation of a continuous unidimensional task with a basis function reinforcement learning model. In model-based fMRI analyses, we found doubly dissociated representations along the hippocampal long axis: state-wise reward prediction error signals in the PH (tail) and global value maximum signals in the AH (anterior body). PH prediction error signals predicted exploration whereas AH global value maximum signals predicted exploitation. AH-mediated exploitation depended on value representations compressed across episodes and options. PH responses to reinforcement were early and phasic while AH responses were delayed and evolved throughout learning. During choice, AH (head) displayed goal cell-like responses to the global value maximum. In summary, granular reinforcement representations in PH facilitate exploration and compressed representations of the value maximum in AH facilitate exploitation.

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Involvement of hippocampal subfields and anterior-posterior subregions in encoding and retrieval of item, spatial, and associative memories: Longitudinal versus transverse axis

Cited by 45 publications

References 174 publications

Neural substrates of mnemonic discrimination: A whole‐brain fMRI investigation

Neural substrates of mnemonic discrimination: A whole‐brain fMRI investigation

Differential Functional Connectivity in Anterior and Posterior Hippocampus Supporting the Development of Memory Formation

Differential reinforcement encoding along the hippocampal long axis helps resolve the explore/exploit dilemma

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