Brain activity during the encoding, retention, and retrieval of stimulus representations.

Studies of delayed nonmatching-to-sample (DNMS) performance following lesions of the monkey cortex have revealed a critical circuit of brain regions involved in forming memories and retaining and retrieving stimulus representations. Using event-related functional magnetic resonance imaging (fMRI), we measured brain activity in 10 healthy human participants during performance of a trial-unique visual DNMS task using novel barcode stimuli. The event-related design enabled the identification of activity during the different phases of the task (encoding, retention, and retrieval). Several brain regions identified by monkey studies as being important for successful DNMS performance showed selective activity during the different phases, including the mediodorsal thalamic nucleus (encoding), ventrolateral prefrontal cortex (retention), and perirhinal cortex (retrieval). Regions showing sustained activity within trials included the ventromedial and dorsal prefrontal cortices and occipital cortex. The present study shows the utility of investigating performance on tasks derived from animal models to assist in the identification of brain regions involved in human recognition memory.

[1]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[2]  M. Mishkin,et al.  Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys , 1997, Neuropsychologia.

[3]  R N Henson,et al.  Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. , 2001, Brain : a journal of neurology.

[4]  R. Turner,et al.  Characterization and Correction of Interpolation Effects in the Realignment of fMRI Time Series , 2000, NeuroImage.

[5]  K. Rockland,et al.  Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas , 2000, The Journal of comparative neurology.

[6]  L. Squire,et al.  Remembering the hippocampus , 1999, Behavioral and Brain Sciences.

[7]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[8]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[9]  L. Squire,et al.  Contrasting Effects on Discrimination Learning after Hippocampal Lesions and Conjoint Hippocampal–Caudate Lesions in Monkeys , 2000, The Journal of Neuroscience.

[10]  Mark W. Greenlee,et al.  Brain regions involved in spatial frequency discrimination: evidence from fMRI , 2000, Experimental Brain Research.

[11]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[12]  E. Koechlin,et al.  Dissociating the role of the medial and lateral anterior prefrontal cortex in human planning. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Larry R. Squire,et al.  CHAPTER 6 – THE NEUROLOGY OF MEMORY: THE CASE FOR CORRESPONDENCE BETWEEN THE FINDINGS FOR HUMAN AND NONHUMAN PRIMATE1 , 1983 .

[14]  M. Mishkin,et al.  Effects of Neonatal Inferior Prefrontal and Medial Temporal Lesions on Learning the Rule for Delayed Nonmatching-to-Sample , 2000, Developmental neuropsychology.

[15]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[16]  E. Murray Memory for objects in nonhuman primates , 2000 .

[17]  P. Reber,et al.  Contrasting cortical activity associated with category memory and recognition memory. , 1998, Learning & memory.

[18]  S. Magnussen Low-level memory processes in vision , 2000, Trends in Neurosciences.

[19]  Seth J. Ramus,et al.  Dissociation between the effects of damage to perirhinal cortex and area TE. , 1999, Learning & memory.

[20]  G. W. Hoesen Anatomy of the medial temporal lobe , 1995 .

[21]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[22]  Randy L. Buckner,et al.  Set-and Code-Specific Activation in the Frontal Cortex: An fMRI Study of Encoding and Retrieval of Faces and Words , 1999, Journal of Cognitive Neuroscience.

[23]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[24]  M D'Esposito,et al.  The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[26]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[27]  E. J. Tehovnik,et al.  Eye fields in the frontal lobes of primates , 2000, Brain Research Reviews.

[28]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[29]  Mortimer Mishkin,et al.  The role of the inferior prefrontal convexity in performance of delayed nonmatching-to-sample , 1991, Neuropsychologia.

[30]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[31]  J. Gallant,et al.  A Human Extrastriate Area Functionally Homologous to Macaque V4 , 2000, Neuron.

[32]  R. Elliott,et al.  Differential Neural Responses during Performance of Matching and Nonmatching to Sample Tasks at Two Delay Intervals , 1999, The Journal of Neuroscience.

[33]  Endel Tulving,et al.  What do animal models of memory model? , 1994, Behavioral and Brain Sciences.

[34]  T. Shallice,et al.  “Sculpting the Response Space”—An Account of Left Prefrontal Activation at Encoding , 2000, NeuroImage.

[35]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[36]  R. Passingham,et al.  Ventral Prefrontal Cortex Is Not Essential for Working Memory , 1997, The Journal of Neuroscience.

[37]  P. O. Bishop,et al.  Spatial vision. , 1971, Annual review of psychology.

[38]  L R Squire,et al.  Perception and recognition memory in monkeys following lesions of area TE and perirhinal cortex. , 2000, Learning & memory.

[39]  N. Sadato,et al.  Functional asymmetry of human prefrontal cortex in verbal and non-verbal episodic memory as revealed by fMRI. , 2000, Brain research. Cognitive brain research.

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

[41]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

[43]  L. Squire,et al.  Functional Magnetic Resonance Imaging (fMRI) Activity in the Hippocampal Region during Recognition Memory , 2000, The Journal of Neuroscience.

[44]  S. Gutnikov,et al.  Perceptual and Mnemonic Matching-To-Sample in Humans: Contributions of The Hippocampus, Perirhinal and Other Medial Temporal Lobe Cortices , 2000, Cortex.

[45]  M Petrides,et al.  Orbitofrontal cortex: A key prefrontal region for encoding information. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[47]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[48]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[49]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  A. Mayes,et al.  Amnesia in a patient with lesions limited to the dorsomedial thalamic nucleus , 1998 .

[51]  L. Squire,et al.  FMRI activity in the medial temporal lobe during recognition memory as a function of study‐test interval , 2000, Hippocampus.

[52]  M. Mishkin,et al.  Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[53]  M. Goldberg,et al.  Neurons in monkey prefrontal cortex that track past or predict future performance. , 2000, Science.

[54]  R. Clark,et al.  Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region , 2000, The Journal of Neuroscience.

[55]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[56]  Daniel S. O'Leary,et al.  Novel vs. Well-learned Memory for Faces: A Positron Emission Tomography Study , 2000, Journal of Cognitive Neuroscience.