Dissociated pathways for successful memory retrieval from the human parietal cortex: anatomical and functional connectivity analyses.

The parietal cortex has traditionally been implicated in spatial attention and eye-movement processes. Recent functional neuroimaging studies have found that activation in the parietal cortex is related to successful recognition memory. The activated regions consistently include the intraparietal sulcus in the lateral parietal cortex and the precuneus in the medial parietal cortex. However, little is known about the functional differences between lateral and medial parietal cortices in the memory retrieval process. In this study, we examined whether the human lateral and medial parietal lobes have differential anatomical and functional connectivity with the temporal lobe. To this end, we used functional magnetic resonance imaging to constrain the analysis of anatomical connectivity obtained by diffusion tensor imaging (DTI). Both DTI tractography and functional connectivity analysis showed that the lateral parietal region has anatomical and functional connections with the lateral temporal lobe, and the medial parietal region has connections with the medial temporal lobe. These results suggest the existence of segregated lateral and medial parieto-temporal pathways in successful memory retrieval.

[1]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[2]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[3]  Sheng He,et al.  Anatomical correlates of the functional organization in the human occipitotemporal cortex. , 2006, Magnetic resonance imaging.

[4]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[5]  M. Mesulam.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  A. Dale,et al.  Functional–Anatomic Study of Episodic Retrieval II. Selective Averaging of Event-Related fMRI Trials to Test the Retrieval Success Hypothesis , 1998, NeuroImage.

[7]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[8]  John S. Duncan,et al.  Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo , 2003, NeuroImage.

[9]  J. S. Snowden,et al.  Semantic dementia: Autobiographical contribution to preservation of meaning , 1995 .

[10]  L. Squire,et al.  The Neuropsychology of Memory , 1990 .

[11]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[12]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

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

[14]  Richard J. Brown.  Neuropsychology Mental Structure , 1989 .

[15]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

[16]  Andy C. H. Lee,et al.  “Pray or Prey?” Dissociation of Semantic Memory Retrieval from Episodic Memory Processes Using Positron Emission Tomography and a Novel Homophone Task , 2002, NeuroImage.

[17]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[19]  M. Rugg,et al.  Separating the Brain Regions Involved in Recollection and Familiarity in Recognition Memory , 2005, The Journal of Neuroscience.

[20]  Anthony D Wagner,et al.  Memory orientation and success: separable neurocognitive components underlying episodic recognition , 2003, Neuropsychologia.

[21]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  D. Stuss,et al.  Neuropsychological studies of the frontal lobes. , 1984, Psychological bulletin.

[23]  R. Buckner,et al.  Functional Dissociation among Components of Remembering: Control, Perceived Oldness, and Content , 2003, The Journal of Neuroscience.

[24]  T. P. S. Powell,et al.  The organization of the cortico-cortical connections between the walls of the lower part of the superior temporal sulcus and the inferior parietal lobule in the monkey , 1988, Brain Research.

[25]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[26]  Dae-Shik Kim,et al.  Diffusion tensor studies dissociated two fronto-temporal pathways in the human memory system , 2007, NeuroImage.

[27]  Christos Davatzikos,et al.  A Framework for Callosal Fiber Distribution Analysis , 2002, NeuroImage.

[28]  J. Hyvärinen.  Posterior parietal lobe of the primate brain. , 1982, Physiological reviews.

[29]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[30]  Timothy Edward John Behrens,et al.  Connection patterns distinguish 3 regions of human parietal cortex. , 2006, Cerebral cortex.

[31]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[32]  G. Micheletti.  The Prefrontal Cortex. Anatomy, Physiology and Neuropsychology of the Frontal Lobe, Fuster J.M.. Raven Press, New York (1989) , 1989 .

[33]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[34]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[35]  A. Alexander,et al.  White matter tractography using diffusion tensor deflection , 2003, Human brain mapping.

[36]  B. Wandell,et al.  Functional organization of human occipital-callosal fiber tracts. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[38]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[39]  J. B. Demb,et al.  Semantic Repetition Priming for Verbal and Pictorial Knowledge: A Functional MRI Study of Left Inferior Prefrontal Cortex , 1997, Journal of Cognitive Neuroscience.

[40]  R. Buckner,et al.  Dissociating State and Item Components of Recognition Memory Using fMRI , 2001, NeuroImage.

[41]  D. Parker,et al.  Analysis of partial volume effects in diffusion‐tensor MRI , 2001, Magnetic resonance in medicine.

[42]  R. Henson,et al.  Neural correlates of retrieval processing in the prefrontal cortex during recognition and exclusion tasks , 2003, Neuropsychologia.

[43]  D. N. Pandya,et al.  The distribution of posterior parietal fibers in the corpus callosum of the rhesus monkey , 2004, Experimental Brain Research.

[44]  Alison R Preston,et al.  Hippocampal contribution to the novel use of relational information in declarative memory , 2004, Hippocampus.

[45]  G. Leichnetz.  Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

[46]  A. Yonelinas.  The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[47]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

[48]  J. Fuster.  The Prefrontal Cortex , 1997 .

[49]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. Schacter.  Memory, amnesia, and frontal lobe dysfunction , 1987, Psychobiology.

[51]  L. Squire.  Declarative and Nondeclarative Memory: Multiple Brain Systems Supporting Learning and Memory , 1992, Journal of Cognitive Neuroscience.

[52]  Gurindar S. Sohi,et al.  Memory systems , 1996, CSUR.

[53]  Andrew L. Alexander,et al.  Bootstrap white matter tractography (BOOT-TRAC) , 2005, NeuroImage.

[54]  Jane E Herron,et al.  Probability effects on the neural correlates of retrieval success: an fMRI study , 2004, NeuroImage.

[55]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[56]  Geoff J. M. Parker,et al.  Characterizing function–structure relationships in the human visual system with functional MRI and diffusion tensor imaging , 2004, NeuroImage.

[57]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[58]  T. P. S. Powell,et al.  The connections of area PG, 7a, with cortex in the parietal, occipital and temporal lobes of the monkey , 1990, Brain Research.

[59]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[60]  M. Mesulam,et al.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[61]  P. Skudlarski,et al.  Brain Connectivity Related to Working Memory Performance , 2006, The Journal of Neuroscience.

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

[63]  Kenichi Ohki,et al.  The role of the parahippocampal gyrus in source memory for external and internal events , 2002, Neuroreport.

[64]  Michael Petrides,et al.  Frontal lobes and behaviour , 1994, Current Opinion in Neurobiology.

[65]  G. Pearlson,et al.  Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem , 2001, NeuroImage.

[66]  Rugg,et al.  Recollection and familiarity in recognition memory: an event-related fMRI study , 1999 .

[67]  Benjamin J. Shannon,et al.  Functional-Anatomic Correlates of Memory Retrieval That Suggest Nontraditional Processing Roles for Multiple Distinct Regions within Posterior Parietal Cortex , 2004, The Journal of Neuroscience.

[68]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[69]  Mario Liotti,et al.  Semantic Amnesia with Preservation of Autobiographic Memory. A Case Report , 1987, Cortex.

[70]  S. Lehéricy,et al.  3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. , 2004, Cerebral cortex.

[71]  D. Neary,et al.  Semantic dementia: a form of circumscribed cerebral atrophy , 1995 .

[72]  P. Boesiger,et al.  SENSE‐DTI at 3 T , 2004, Magnetic resonance in medicine.

[73]  Pierre Maquet,et al.  Brain activity underlying encoding and retrieval of source memory. , 2002, Cerebral cortex.

[74]  Elisa C. Dias,et al.  Cortical afferents to the smooth-pursuit region of the macaque monkey’s frontal eye field , 2005, Experimental Brain Research.

[75]  John S. Duncan,et al.  Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus , 2004, NeuroImage.

[76]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[77]  Roberto Cabeza,et al.  Neural Correlates of Relational Memory: Successful Encoding and Retrieval of Semantic and Perceptual Associations , 2005, The Journal of Neuroscience.

[78]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[79]  H G Wieser,et al.  Human hippocampus associates information in memory. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[80]  J. Lynch,et al.  Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys. , 1996, Journal of neurophysiology.

[81]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[82]  Koji Jimura,et al.  Activation shift from medial to lateral temporal cortex associated with recency judgements following impoverished encoding. , 2006, Cerebral cortex.

[83]  Sterling C. Johnson,et al.  Application of Brodmann's area templates for ROI selection in white matter tractography studies , 2006, NeuroImage.

[84]  D. Schnyer,et al.  A critical role for the anterior hippocampus in relational memory: Evidence from an fMRI study comparing associative and item recognition , 2004, Hippocampus.

[85]  K J Friston,et al.  The predictive value of changes in effective connectivity for human learning. , 1999, Science.

[86]  John Hart,et al.  Delineation of single‐word semantic comprehension deficits in aphasia, with anatomical correlation , 1990, Annals of neurology.

[87]  O. Krastoshevsky,et al.  Hippocampal Contributions to Episodic Encoding : Insights From Relational and Item-Based Learning , 2002 .

[88]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[89]  Alex Martin,et al.  Neural correlates of semantic and episodic memory retrieval , 1998, Neuropsychologia.

[90]  G. Rees,et al.  Covariation of activity in visual and prefrontal cortex associated with subjective visual perception. , 1999, Proceedings of the National Academy of Sciences of the United States of America.