Involvement of the human medial temporal lobe in a visual discrimination task

Recent imaging and lesion studies suggest that the human medial temporal lobe (including the hippocampus and the perirhinal cortex), which is traditionally believed to be of central importance for memory processing, is also involved in processing and discrimination of complex visual stimuli. The aim of this study was to use functional magnetic resonance imaging in healthy subjects to further elucidate the contributions of different medial temporal lobe structures to perceptual and mnemonic processing of faces and scenes, by directly comparing the activation in a visual discrimination and a recognition task (one week after encoding). A within-subjects full factorial analysis revealed significant hippocampal activation for both discrimination and recognition task, with no differential activations for the processing of faces or scenes. No perirhinal activation was found in either of the experimental conditions. These results support a perceptual-mnemonic theory of the medial temporal lobe, while questioning a simple mapping of different functions to single structures like hippocampus and perirhinal cortex.

[1]  Andy C. H. Lee,et al.  Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of viewpoint , 2009, Hippocampus.

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

[3]  Andy C. H. Lee,et al.  Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception , 2010, Neuropsychologia.

[4]  Boris Suchan,et al.  Hippocampal involvement in recollection but not familiarity across time: A prospective study , 2008, Hippocampus.

[5]  B. Staresina,et al.  Mind the Gap: Binding Experiences across Space and Time in the Human Hippocampus , 2009, Neuron.

[6]  Lisa M Saksida,et al.  The Perceptual-Mnemonic/Feature Conjunction Model of Perirhinal Cortex Function , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[7]  C. Price,et al.  Perirhinal Contributions to Human Visual Perception , 2007, Current Biology.

[8]  L. Saksida,et al.  Object memory and perception in the medial temporal lobe: an alternative approach , 2005, Current Opinion in Neurobiology.

[9]  Elisabeth A. Murray,et al.  What, if anything, is the medial temporal lobe, and how can the amygdala be part of it if there is no such thing? , 2004, Neurobiology of Learning and Memory.

[10]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[11]  Robert R Hampton,et al.  Monkey Perirhinal Cortex is Critical for Visual Memory, but not for Visual Perception: Reexamination of the Behavioural Evidence from Monkeys , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[12]  Matthew H Tong,et al.  Why is the fusiform face area recruited for novel categories of expertise? A neurocomputational investigation , 2008, Brain Research.

[13]  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.

[14]  M. Buckley.  The Role of the Perirhinal Cortex and Hippocampus in Learning, Memory, and Perception , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[15]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[16]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[17]  wen ling ma,et al.  Behavioural Brain Research , 2016 .

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

[19]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Projections to the neocortex , 2002, The Journal of comparative neurology.

[20]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[21]  William A. Cunningham,et al.  Type I and Type II error concerns in fMRI research: re-balancing the scale. , 2009, Social cognitive and affective neuroscience.

[22]  Andy C. H. Lee,et al.  Behavioral / Systems / Cognitive Functional Specialization in the Human Medial Temporal Lobe , 2005 .

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

[24]  Larry R Squire,et al.  Intact Working Memory for Relational Information after Medial Temporal Lobe Damage , 2010, The Journal of Neuroscience.

[25]  Andy C. H. Lee,et al.  Activating the medial temporal lobe during oddity judgment for faces and scenes. , 2008, Cerebral cortex.

[26]  C. Price,et al.  Integrating Visual and Tactile Information in the Perirhinal Cortex , 2009, Cerebral cortex.

[27]  L. Davachi,et al.  Distortion and Signal Loss in Medial Temporal Lobe , 2009, PloS one.

[28]  Neal J. Cohen,et al.  Processing and short-term retention of relational information in amnesia , 2004, Neuropsychologia.

[29]  Wendy A. Suzuki,et al.  Perception and the Medial Temporal Lobe: Evaluating the Current Evidence , 2009, Neuron.

[30]  L. Squire,et al.  Intact visual discrimination of complex and feature-ambiguous stimuli in the absence of perirhinal cortex. , 2005, Learning & memory.

[31]  N. Kanwisher.  Domain specificity in face perception , 2000, Nature Neuroscience.

[32]  L. Saksida,et al.  Memory, perception, and the ventral visual‐perirhinal‐hippocampal stream: Thinking outside of the boxes , 2007, Hippocampus.

[33]  L. Squire,et al.  The cognitive neuroscience of human memory since H.M. , 2011, Annual review of neuroscience.

[34]  Heather L. Urry,et al.  Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression , 2007, The Journal of Neuroscience.

[35]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

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

[37]  Daniel L. Schacter,et al.  The nature of memory related activity in early visual areas , 2006, Neuropsychologia.

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

[39]  Richard N. A. Henson,et al.  Perception and Conception: Temporal Lobe Activity during Complex Discriminations of Familiar and Novel Faces and Objects , 2011, Journal of Cognitive Neuroscience.

[40]  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.

[41]  L. Saksida,et al.  Visual perception and memory: a new view of medial temporal lobe function in primates and rodents. , 2007, Annual review of neuroscience.

[42]  Russell A. Epstein,et al.  Perceptual deficits in amnesia: challenging the medial temporal lobe ‘mnemonic’ view , 2005, Neuropsychologia.

[43]  L. Saksida,et al.  Perirhinal cortex resolves feature ambiguity in complex visual discriminations , 2002, The European journal of neuroscience.

[44]  L. Squire,et al.  Memory, Visual Discrimination Performance, and the Human Hippocampus , 2011, The Journal of Neuroscience.

[45]  William A. Cunningham,et al.  Tools of the Trade Type I and Type II error concerns in fMRI research : rebalancing the scale , 2009 .

[46]  Demis Hassabis,et al.  Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI , 2011, Learning & memory.

[47]  Edward B. O'Neil,et al.  Perirhinal Cortex Contributes to Accuracy in Recognition Memory and Perceptual Discriminations , 2009, The Journal of Neuroscience.

[48]  Erik D. Flister,et al.  Intact Performance on Feature-Ambiguous Discriminations in Rats with Lesions of the Perirhinal Cortex , 2011, Neuron.

[49]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[50]  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.

[51]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[52]  B. Staresina,et al.  Perirhinal and Parahippocampal Cortices Differentially Contribute to Later Recollection of Object- and Scene-Related Event Details , 2011, The Journal of Neuroscience.

[53]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[54]  Soojin Park,et al.  Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception , 2009, NeuroImage.

[55]  Andy C. H. Lee,et al.  Human Medial Temporal Lobe Damage Can Disrupt the Perception of Single Objects , 2010, The Journal of Neuroscience.

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

[57]  L. Squire,et al.  Intact visual perceptual discrimination in humans in the absence of perirhinal cortex. , 2000, Learning & memory.

[58]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[60]  B. Suchan,et al.  The medial temporal lobe: Memory and beyond , 2013, Behavioural Brain Research.

[61]  I. Daum,et al.  Human memory manipulated: Dissociating factors contributing to MTL activity, an fMRI study , 2012, Behavioural Brain Research.

[62]  C. Ranganath.  A unified framework for the functional organization of the medial temporal lobes and the phenomenology of episodic memory , 2010, Hippocampus.

[63]  Jamil Zaki,et al.  Overlapping activity in anterior insula during interoception and emotional experience , 2012, NeuroImage.