Functional interactions between the medial temporal lobes and posterior neocortex related to episodic memory retrieval.

We applied structural equation modeling to positron emission tomography data in humans to examine functional interactions between the right medial temporal lobe (MTL) and selected right neocortical regions in relation to visual recognition memory. Using a priori knowledge about anatomical connections between these regions as a guiding constraint, we modeled the pattern of interactions [i.e. covariances in regional cerebral blood flow (rCBF)] associated with episodic memory retrieval of spatial location and compared it with the pattern for retrieval of object identity. We also compared these patterns with those associated with perceptual matching of spatial location and object identity. Although displaying no difference in average rCBF across tasks, the right MTL showed domain-specific qualitative differences in interactions with posterior dorsal (parieto-occipital sulcus, supramarginal gyrus) and ventral regions (fusiform gyrus, superior temporal sulcus) but not with a prefrontal region. MTL interactions involving dorsal regions were positive in the spatial retrieval task but negative for object retrieval. Interactions involving ventral regions showed the reverse pattern. No comparable changes were observed during perceptual matching. Using control models, we demonstrated the neuroanatomical specificity of these results. Our results provide support for the notion that the nature of interactions between the MTL and posterior neocortex depends on the domain of information to-be-recovered.

[1]  S. Grossberg,et al.  Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions , 1993, Trends in Neurosciences.

[2]  Marilyn Jones-Gotman,et al.  Right hippocampal excision impairs learning and recall of a list of abstract designs , 1986, Neuropsychologia.

[3]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Renzi,et al.  Spatial Memory and Hemispheric Locus of Lesion , 1977, Cortex.

[5]  Karl Magnus Petersson,et al.  A Dynamic Role of the Medial Temporal Lobe during Retrieval of Declarative Memory in Man , 1997, NeuroImage.

[6]  Richard S. J. Frackowiak,et al.  Learning to find your way: a role for the human hippocampal formation , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  Karl G. Jöreskog,et al.  Lisrel 8: Structural Equation Modeling With the Simplis Command Language , 1993 .

[9]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[10]  A. Damasio Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition , 1989, Cognition.

[11]  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.

[12]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

[13]  T. Teyler,et al.  The hippocampal memory indexing theory. , 1986, Behavioral neuroscience.

[14]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[15]  B. Milner Amnesia following operation on the temporal lobes , 1996 .

[16]  E. Tulving,et al.  PET studies of encoding and retrieval: The HERA model , 1996, Psychonomic bulletin & review.

[17]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[18]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[19]  Jan Voogd,et al.  The human central nervous system : a synopsis and atlas , 1978 .

[20]  Brenda Milner,et al.  The role of the right hippocampus in the recall of spatial location , 1981, Neuropsychologia.

[21]  Arthur P. Shimamura,et al.  Memory and frontal lobe function. , 1995 .

[22]  Leslie G. Ungerleider,et al.  Network analysis of cortical visual pathways mapped with PET , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[24]  Daniel L. Schacter,et al.  Brain regions associated with retrieval of structurally coherent visual information , 1995, Nature.

[25]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[26]  M. Moscovitch,et al.  Distinct neural correlates of visual long-term memory for spatial location and object identity: a positron emission tomography study in humans. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[27]  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 .

[28]  Elisabeth A. Murray,et al.  What have ablation studies told us about the neural substrates of stimulus memory , 1996 .

[29]  Alan C. Evans,et al.  Memory for object-features versus memory for object-location: A positron emission tomography study of encoding and retrieval processes , 1996, NeuroImage.

[30]  J. Voogd,et al.  The human central nervous system , 1978 .

[31]  J. Bullier,et al.  Functional streams in occipito-frontal connections in the monkey , 1996, Behavioural Brain Research.

[32]  D. Kimura Right temporal-lobe damage. Perception of unfamiliar stimuli after damage. , 1963, Archives of neurology.

[33]  Brenda Milner,et al.  Memory for different aspects of complex visual scenes after unilateral temporal- or frontal-lobe resection , 1993, Neuropsychologia.

[34]  M Moscovitch,et al.  Recovered consciousness: a hypothesis concerning modularity and episodic memory. , 1995, Journal of clinical and experimental neuropsychology.

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

[36]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

[37]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[38]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  S. Black,et al.  Memory impairments associated with hippocampal versus parahippocampal-gyrus atrophy: an MR volumetry study in Alzheimer’s disease , 1998, Neuropsychologia.

[40]  Scott T. Grafton,et al.  Network analysis of motor system connectivity in Parkinson's disease: Modulation of thalamocortical interactions after pallidotomy , 1994 .

[41]  Morris Moscovitch,et al.  The neuropsychology of memory and aging. , 1992 .

[42]  Morris Moscovitch,et al.  Networks of domain-specific and general regions involved in episodic memory for spatial location and object identity , 1998, Neuropsychologia.

[43]  C. Frith,et al.  The functional neuroanatomy of episodic memory , 1997, Trends in Neurosciences.

[44]  L. Nadel,et al.  The medial temporal region and memory consolidation: A new hypothesis , 2014 .

[45]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[46]  Leslie G. Ungerleider,et al.  Changes in limbic and prefrontal functional interactions in a working memory task for faces. , 1996, Cerebral cortex.

[47]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[48]  A. Pickering,et al.  Spatial memory deficits in patients with unilateral damage to the right hippocampal formation , 1997, Neuropsychologia.

[49]  Alan C. Evans,et al.  A Specific Role for the Right Parahippocampal Gyrus in the Retrieval of Object-Location: A Positron Emission Tomography Study , 1996, Journal of Cognitive Neuroscience.

[50]  E. Tulving,et al.  Network Analysis of Positron Emission Tomography Regional Cerebral Blood Flow Data: Ensemble Inhibition during Episodic Memory Retrieval , 1996, The Journal of Neuroscience.

[51]  G. Winocur,et al.  Dissociation of pathways for object and spatial vision: a PET study in humans , 1995, Neuroreport.

[52]  A R McIntosh,et al.  Functional brain maps of retrieval mode and recovery of episodic information , 1995, Neuroreport.

[53]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[54]  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.

[55]  N. Alpert,et al.  Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Brenda Milner,et al.  Visual recognition and recall after right temporal-lobe excision in man , 1968 .

[57]  F L Bookstein,et al.  Differential functional connectivity of prefrontal and medial temporal cortices during episodic memory retrieval , 1997, Human brain mapping.

[58]  Robert T. Knight,et al.  Prefrontal cortex gating of auditory transmission in humans , 1989, Brain Research.

[59]  Morris Moscovitch,et al.  Modularity and neuropsychology: Modules and central processes in attention and memory. , 1990 .

[60]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[61]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[62]  Cheryl L. Grady,et al.  Functional Associations among Human Posterior Extrastriate Brain Regions during Object and Spatial Vision , 1992, Journal of Cognitive Neuroscience.

[63]  Karl J. Friston,et al.  Commentary and Opinion: II. Statistical Parametric Mapping: Ontology and Current Issues , 1995, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[64]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[65]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[66]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[67]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[68]  G. Orban,et al.  Positron-emission tomography imaging of long-term shape recognition challenges. , 1997, Proceedings of the National Academy of Sciences of the United States of America.