Neuroanatomical correlates of implicit and explicit memory for structurally possible and impossible visual objects.

Implicit memory refers to nonconscious retrieval of past experience demonstrated by facilitation in test performance on tasks that do not require intentional recollection of previous experiences. Explicit memory, in contrast, refers to the conscious retrieval of prior information, as demonstrated during standard recall and recognition tasks. In this experiment, positron emission tomographic (PET) measurements of regional cerebral blood flow (CBF), a marker of local neuronal activity, were used to identify and contrast brain regions that participate in the perception, implicit memory, and explicit memory for structurally possible and impossible visual objects. Ten CBF images were acquired in 16 normal women as they made possible/impossible and old/new recognition decisions about previously studied (old) and nonstudied (new) structurally possible and impossible objects. As reported previously, object decisions for familiar possible objects were associated with increased CBF in the vicinity of the left inferior temporal and fusiform gyri and recognition memory for familiar possible objects was associated with increased CBF in the vicinity of the right hippocampus. In this report, we provide more extensive analyses of the roles of the inferior temporal cortex, the hippocampus, the parahippocampus, and the pulvinar in encoding and retrieval operations. Additionally, patterns of CBF increases and decreases provide information regarding the neural structures involved in implicit and explicit memory.

[1]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[2]  P E Roland,et al.  Visual form discrimination from color or motion cues: functional anatomy by positron emission tomography. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[6]  E. Tulving,et al.  Memory Systems 1994 , 1994 .

[7]  L. Cooper,et al.  Implicit memory for possible and impossible objects: constraints on the construction of structural descriptions. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

[8]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[11]  R. Dolan,et al.  Brain regions supporting intentional and incidental memory: a PET study , 1997, Neuroreport.

[12]  Daniel L. Schacter,et al.  Neuroanatomical Correlates of Veridical and Illusory Recognition Memory: Evidence from Positron Emission Tomography , 1996, Neuron.

[13]  D. LaBerge,et al.  Theory of attentional operations in shape identification. , 1989 .

[14]  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.

[15]  L. Cooper,et al.  Preserved Priming of Novel Objects across Size Transformation in Amnesic Patients , 1993 .

[16]  D. Schacter,et al.  Implicit and explicit memory for new associations in normal and amnesic subjects. , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[17]  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.

[18]  B. Milner,et al.  Psychological defects produced by temporal lobe excision. , 1958, Research publications - Association for Research in Nervous and Mental Disease.

[19]  A. Kertesz,et al.  The Structural Determinants of Recovery in Wernicke′s Aphasia , 1993, Brain and Language.

[20]  G. Humphreys,et al.  Visual object processing in optic aphasia: a case of semantic access agnosia , 1987 .

[21]  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.

[22]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[23]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[24]  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.

[25]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[26]  M. Mesulam Principles of behavioral neurology , 1985 .

[27]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[29]  T. Shallice Specific impairments of planning. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  P. Goldman-Rakic Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[31]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[32]  D. V. van Essen,et al.  A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  E. Courchesne,et al.  A new role for the cerebellum in cognitive operations. , 1992, Behavioral neuroscience.

[34]  D. Schacter Implicit memory: History and current status. , 1987 .

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

[36]  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.

[37]  Daniel L. Schacter,et al.  Priming and recognition of transformed three-dimensional objects: effects of size and reflection. , 1992 .

[38]  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.

[39]  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.

[40]  P. E. Roland,et al.  Mapping of Learning and Memory Functions in the Human Brain , 1989 .

[41]  M. Posner,et al.  Localization of cognitive operations in the human brain. , 1988, Science.

[42]  J M Wyss,et al.  An autoradiographic study of the efferent connections of the entorhinal cortex in the rat , 1981, The Journal of comparative neurology.

[43]  D L Schacter,et al.  Implicit and explicit memory for novel visual objects: structure and function. , 1993, Journal of experimental psychology. Learning, memory, and cognition.

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

[45]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[46]  P E Roland,et al.  Does mental activity change the oxidative metabolism of the brain? , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  H. Roediger Implicit memory in normal human subjects , 1993 .

[48]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[49]  Daniel L. Schacter,et al.  Preserved Priming of Novel Objects in Patients with Memory Disorders , 1991, Journal of Cognitive Neuroscience.

[50]  D L Schacter,et al.  Effects of size and orientation change on hippocampal activation during episodic recognition: A PET study , 1997, Neuroreport.

[51]  A. Damasio,et al.  Neural regionalization of knowledge access: preliminary evidence. , 1990, Cold Spring Harbor symposia on quantitative biology.

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

[53]  Robert A. Bjork,et al.  Measures of Memory , 1988 .

[54]  D. Willingham Systems of Memory in the Human Brain , 1997, Neuron.

[55]  M P Witter,et al.  Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat , 1984, The Journal of comparative neurology.

[56]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[57]  L. Cooper,et al.  Implicit memory for unfamiliar objects depends on access to structural descriptions , 1990 .

[58]  D. LaBerge,et al.  Positron emission tomographic measurements of pulvinar activity during an attention task , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[61]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

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

[63]  A. Damasio Category-related recognition defects as a clue to the neural substrates of knowledge , 1990, Trends in Neurosciences.

[64]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  M. J. Riddoch,et al.  Visual object processing in optic aphasia: a case of semantic access agnosia , 1987 .

[66]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[67]  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.

[68]  A. Dale,et al.  Late Onset of Anterior Prefrontal Activity during True and False Recognition: An Event-Related fMRI Study , 1997, NeuroImage.

[69]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[70]  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 .

[71]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[72]  E. Tulving,et al.  Novelty encoding networks in the human brain: positron emission tomography data. , 1994, Neuroreport.

[73]  S. Petersen,et al.  Impaired non-motor learning and error detection associated with cerebellar damage. A single case study. , 1992, Brain : a journal of neurology.

[74]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

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

[76]  Peter Graf,et al.  Implicit Memory : New Directions in Cognition, Development, and Neuropsychology , 1993 .

[77]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

[79]  Morris Moscovitch,et al.  Memory and working with memory: Evaluation of a component process model and comparisons with other models. , 1994 .

[80]  D. Schacter,et al.  Implicit and explicit memory for new associations in normal and amnesic subjects. , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[81]  Karl J. Friston,et al.  A graded task approach to the functional mapping of brain areas implicated in auditory-verbal memory. , 1994, Brain : a journal of neurology.

[82]  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.

[83]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[84]  W. Nauta THE PROBLEM OF THE FRONTAL LOBE: A REINTERPRETATION , 1972 .

[85]  D. Schacter,et al.  Implicit memory: a selective review. , 1993, Annual review of neuroscience.