Performance-Related Sustained and Anticipatory Activity in Human Medial Temporal Lobe during Delayed Match-to-Sample

The medial temporal lobe (MTL)—hippocampus and surrounding perirhinal, parahippocampal, and entorhinal cortical areas—has long been known to be critical for long-term memory for events. Recent functional neuroimaging and neuropsychological data in humans performing short-delay tasks suggest that the MTL also contributes to performance even when retention intervals are brief, and single-unit data in rodents reveal sustained, performance-related delay activity in the MTL during delayed-non-match-to-sample tasks. The current study used functional magnetic resonance imaging to examine the relationship between activation in human MTL subregions and performance during a delayed-match-to-sample task with repeated (non-trial-unique) stimuli. On critical trials, the presentation of two faces was followed by a 30 s delay period, after which participants performed two-alternative forced-choice recognition. Functional magnetic resonance imaging revealed significant delay period activity in anterior hippocampus, entorhinal cortex, and perirhinal cortex over the 30 s retention interval, with the magnitude of activity being significantly higher on subsequently correct compared with subsequently incorrect trials. In contrast, posterior hippocampus, parahippocampal cortex, and fusiform gyrus activity linearly increased across the 30 s delay, suggesting an anticipatory response, and activity in parahippocampal cortex and hippocampus was greater during the probe period on correct compared with incorrect trials. These results indicate that at least two patterns of MTL delay period activation—sustained and anticipatory—are present during performance of short-delay recognition memory tasks, providing novel evidence that multiple processes govern task performance. Implications for understanding the role of the hippocampus and surrounding MTL cortical areas in recognition memory after short delays are discussed.

[1]  Gary H. Glover,et al.  High-resolution fMRI of Content-sensitive Subsequent Memory Responses in Human Medial Temporal Lobe , 2010, Journal of Cognitive Neuroscience.

[2]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[3]  L. Davachi,et al.  Category‐specificity in the human medial temporal lobe cortex , 2009, Hippocampus.

[4]  F. Tong,et al.  Decoding reveals the contents of visual working memory in early visual areas , 2009, Nature.

[5]  Edward F. Ester,et al.  PSYCHOLOGICAL SCIENCE Research Article Stimulus-Specific Delay Activity in Human Primary Visual Cortex , 2022 .

[6]  Michael A Yassa,et al.  A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe , 2009, NeuroImage.

[7]  Lila Davachi,et al.  Distinct Memory Signatures in the Hippocampus: Intentional States Distinguish Match and Mismatch Enhancement Signals , 2009, The Journal of Neuroscience.

[8]  Wendy A. Suzuki,et al.  Comparative analysis of the cortical afferents, intrinsic projections and interconnections of the parahippocampal region in monkeys and rats , 2009 .

[9]  E. Save,et al.  Delay-dependent involvement of the rat entorhinal cortex in habituation to a novel environment , 2008, Neurobiology of Learning and Memory.

[10]  Adam Gazzaley,et al.  Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. , 2008, Cerebral cortex.

[11]  Ramona O Hopkins,et al.  Working Memory and the Organization of Brain Systems , 2008, The Journal of Neuroscience.

[12]  Richard L. Lewis,et al.  The mind and brain of short-term memory. , 2008, Annual review of psychology.

[13]  Charan Ranganath,et al.  Medial Temporal Lobe Activity Predicts Successful Relational Memory Binding , 2008, The Journal of Neuroscience.

[14]  Morgan D. Barense,et al.  The human medial temporal lobe processes online representations of complex objects , 2007, Neuropsychologia.

[15]  Tim Shallice,et al.  Fractionation of memory in medial temporal lobe amnesia , 2007, Neuropsychologia.

[16]  Richard N. A. Henson,et al.  Recognition memory for faces and scenes in amnesia: Dissociable roles of medial temporal lobe structures , 2007, Neuropsychologia.

[17]  R. Kessels,et al.  Spatial and non-spatial contextual working memory in patients with diencephalic or hippocampal dysfunction , 2007, Brain Research.

[18]  Craig K. Jones,et al.  High‐resolution fMRI investigation of the medial temporal lobe , 2007, Human brain mapping.

[19]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[20]  Michael X. Cohen,et al.  Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe , 2007, The Journal of Neuroscience.

[21]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[22]  S. R. Lehky,et al.  Enhancement of object representations in primate perirhinal cortex during a visual working-memory task. , 2007, Journal of neurophysiology.

[23]  N. Burgess,et al.  The hippocampus is required for short‐term topographical memory in humans , 2007, Hippocampus.

[24]  Alison R. Preston,et al.  The medial temporal lobe and memory , 2007 .

[25]  L. Davachi Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

[26]  M. Hasselmo,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.11 Mechanisms underlying working memory for novel information , 2022 .

[27]  Guillén Fernández,et al.  The right hippocampus participates in short-term memory maintenance of object–location associations , 2006, NeuroImage.

[28]  Alex Martin,et al.  Access the most recent version at doi: 10.1101/lm.251906 , 2006 .

[29]  Neal J. Cohen,et al.  The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags , 2006, The Journal of Neuroscience.

[30]  John D E Gabrieli,et al.  Working memory and long‐term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes , 2006, Hippocampus.

[31]  Anjan Chatterjee,et al.  Visual Working Memory Is Impaired when the Medial Temporal Lobe Is Damaged , 2006, Journal of Cognitive Neuroscience.

[32]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[33]  Ingrid R. Olson,et al.  Working Memory for Conjunctions Relies on the Medial Temporal Lobe , 2006, The Journal of Neuroscience.

[34]  Yael Shrager,et al.  Intact Visual Perception in Memory-Impaired Patients with Medial Temporal Lobe Lesions , 2006, The Journal of Neuroscience.

[35]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[36]  Charan Ranganath,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.8 August 2005 Doubts about double dissociations between short- and long-term memory , 2022 .

[37]  Michael X. Cohen,et al.  Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence , 2005, Journal of Cognitive Neuroscience.

[38]  B. Knowlton,et al.  A Dissociation of Encoding and Retrieval Processes in the Human Hippocampus , 2005, The Journal of Neuroscience.

[39]  Janita Turchi,et al.  Effects of cholinergic deafferentation of the rhinal cortex on visual recognition memory in monkeys. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Yaakov Stern,et al.  Positive evidence against human hippocampal involvement in working memory maintenance of familiar stimuli. , 2004, Cerebral cortex.

[41]  Anthony D Wagner,et al.  Conceptual and perceptual novelty effects in human medial temporal cortex , 2005, Hippocampus.

[42]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[43]  M. Hasselmo,et al.  Persistence of Parahippocampal Representation in the Absence of Stimulus Input Enhances Long-Term Encoding: A Functional Magnetic Resonance Imaging Study of Subsequent Memory after a Delayed Match-to-Sample Task , 2004, The Journal of Neuroscience.

[44]  M. D’Esposito,et al.  Functional connectivity during working memory maintenance , 2004, Cognitive, affective & behavioral neuroscience.

[45]  Robert E Hampson,et al.  Differential but Complementary Mnemonic Functions of the Hippocampus and Subiculum , 2004, Neuron.

[46]  Alison R Preston,et al.  Comparison of spiral-in/out and spiral-out BOLD fMRI at 1.5 and 3 T , 2004, NeuroImage.

[47]  E. Rolls,et al.  Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks , 2004, Experimental Brain Research.

[48]  C. Stark,et al.  Making Memories without Trying: Medial Temporal Lobe Activity Associated with Incidental Memory Formation during Recognition , 2003, The Journal of Neuroscience.

[49]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  S. Engel,et al.  Dynamics of the Hippocampus During Encoding and Retrieval of Face-Name Pairs , 2003, Science.

[51]  Alan C. Evans,et al.  Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. , 2002, Cerebral cortex.

[52]  M. Hasselmo,et al.  Graded persistent activity in entorhinal cortex neurons , 2002, Nature.

[53]  G. Glover,et al.  Regularized higher‐order in vivo shimming , 2002, Magnetic resonance in medicine.

[54]  M. Hasselmo,et al.  Simulations of the Role of the Muscarinic-Activated Calcium-Sensitive Nonspecific Cation CurrentINCM in Entorhinal Neuronal Activity during Delayed Matching Tasks , 2002, The Journal of Neuroscience.

[55]  K. Paller,et al.  Observing the transformation of experience into memory , 2002, Trends in Cognitive Sciences.

[56]  G. Glover,et al.  Correction of physiologically induced global off‐resonance effects in dynamic echo‐planar and spiral functional imaging , 2002, Magnetic resonance in medicine.

[57]  R. Clark,et al.  The medial temporal lobe and memory. , 2002 .

[58]  S. Small,et al.  The Longitudinal Axis of the Hippocampal Formation: Its Anatomy, Circuitry, and Role in Cognitive Function , 2002, Reviews in the neurosciences.

[59]  M. D’Esposito,et al.  Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information , 2001, Neuron.

[60]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[61]  Russell A. Epstein,et al.  Neuropsychological evidence for a topographical learning mechanism in parahippocampal cortex , 2001, Cognitive neuropsychology.

[62]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[63]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[64]  E. Murray,et al.  Opposite relationship of hippocampal and rhinal cortex damage to delayed nonmatching‐to‐sample deficits in monkeys † , 2001, Hippocampus.

[65]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[66]  Stephen A. Engel,et al.  Application of Cortical Unfolding Techniques to Functional MRI of the Human Hippocampal Region , 2000, NeuroImage.

[67]  John J. B. Allen,et al.  Memory Deficits Characterized by Patterns of Lesions to the Hippocampus and Parahippocampal Cortex , 2000, Annals of the New York Academy of Sciences.

[68]  Alan C. Evans,et al.  Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. , 2000, Cerebral cortex.

[69]  Leslie G. Ungerleider,et al.  Distinguishing the Functional Roles of Multiple Regions in Distributed Neural Systems for Visual Working Memory , 2000, NeuroImage.

[70]  Leslie G. Ungerleider,et al.  Distinguishing the Functional Roles of Multiple Regions in Distributed Neural Systems for Visual Working Memory , 2000, NeuroImage.

[71]  Leslie G. Ungerleider,et al.  Complementary neural mechanisms for tracking items in human working memory. , 2000, Science.

[72]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[73]  J. Fuster,et al.  From perception to action: temporal integrative functions of prefrontal and parietal neurons. , 1999, Cerebral cortex.

[74]  D. Amaral,et al.  Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 1998 .

[75]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[76]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[77]  M. Mishkin,et al.  Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus , 1998, The Journal of Neuroscience.

[78]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[79]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[80]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[81]  L. Squire,et al.  The human perirhinal cortex and recognition memory , 1998, Hippocampus.

[82]  R. Desimone,et al.  Object and place memory in the macaque entorhinal cortex. , 1997, Journal of neurophysiology.

[83]  H. Eichenbaum,et al.  Memory Representation within the Parahippocampal Region , 1997, The Journal of Neuroscience.

[84]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[85]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[86]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[87]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[88]  M Meunier,et al.  Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. , 1996, Journal of neurophysiology.

[89]  P Alvarez,et al.  Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[91]  E. Murray,et al.  Preserved Recognition Memory for Small Sets, and Impaired Stimulus Identification for Large Sets, Following Rhinal Cortex Ablations in Monkeys , 1994, The European journal of neuroscience.

[92]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[95]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task , 1992 .

[96]  C. B. Cave,et al.  Intact verbal and nonverbal short‐term memory following damage to the human hippocampus , 1992, Hippocampus.

[97]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[98]  E. Murray,et al.  Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. , 1992, Behavioral neuroscience.

[99]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. , 1992, Behavioral neuroscience.

[100]  D. Amaral,et al.  Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex , 1991, The Journal of comparative neurology.

[101]  R. Levine,et al.  Postembryonic neuronal plasticity and its hormonal control during insect metamorphosis. , 1990, Annual review of neuroscience.

[102]  D. Amaral,et al.  Topographical organization of the entorhinal projection to the dentate gyrus of the monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[103]  A M Taylor,et al.  Immediate Memory for Faces: Long- or Short-Term Memory? , 1973, The Quarterly journal of experimental psychology.