The neuroimaging of long-term memory encoding processes.

There needs to be more crosstalk between the lesion and functional neuroimaging memory literatures. This is illustrated by a discussion of episode and fact encoding. The lesion literature suggests several hypotheses about which brain regions underlie the storage of episode and fact information, which can be explored by functional neuroimaging. These hypotheses have been underexplored because neuroimaging studies of encoding have been insufficiently hypothesis-driven and have not controlled encoding-related processes sufficiently well to allow clear interpretations of results to be made. Nevertheless, there is good evidence that certain kinds of associative encoding and/or consolidation are sufficient to activate the medial temporal lobes, and preliminary evidence that some kinds of associative priming may reduce activation of this region. It remains to be proved that attentional orienting to certain kinds of novel information activates the medial temporal lobes. Evidence is growing that the HERA model, developed from neuroimaging rather than lesion data, requires modification and that frontal cortex encoding activations are probably caused by executive processes that are important in effortful memory processing. Neuroimaging studies allow the detection of encoding-related activations in previously unexpected brain regions (e.g. parietal lobes) and, in turn, these findings can be explored with lesion studies.

[1]  Daniel L. Schacter,et al.  On the Relations among Priming, Conscious Recollection, and Intentional Retrieval: Evidence from Neuroimaging Research , 1998, Neurobiology of Learning and Memory.

[2]  D G Gadian,et al.  Amnesia and the organization of the hippocampal system , 1998, Hippocampus.

[3]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[4]  D L Schacter,et al.  Preserved learning in amnesic patients: perspectives from research on direct priming. , 1986, Journal of clinical and experimental neuropsychology.

[5]  J. Deese On the prediction of occurrence of particular verbal intrusions in immediate recall. , 1959, Journal of experimental psychology.

[6]  C D Frith,et al.  The functional roles of prefrontal cortex in episodic memory. II. Retrieval. , 1998, Brain : a journal of neurology.

[7]  R. Knight Contribution of human hippocampal region to novelty detection , 1996, Nature.

[8]  Alex Martin,et al.  Automatic activation of the medial temporal lobe during encoding: Lateralized influences of meaning and novelty , 1999, Hippocampus.

[9]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

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

[11]  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.

[12]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

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

[17]  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.

[18]  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.

[19]  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.

[20]  Kamil Ugurbil,et al.  Monitoring of cerebral multiphasic sustained responses (CMSR) in memory processing using fMRI , 1997 .

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

[22]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  S. E. Petersen,et al.  Response from Kelley, Buckner and Petersen , 1998, Trends in Cognitive Sciences.

[24]  A. Mayes,et al.  Rate of forgetting in amnesia: II. Recall and recognition of word lists at different levels of organization. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[25]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[26]  R. Dolan,et al.  Encoding and retrieval in human medial temporal lobes: An empirical investigation using functional magnetic resonance imaging (fMRI) , 1999, Hippocampus.

[27]  C. Laurent-Demir,et al.  Temporally extended retrograde amnesia for spatial information resulting from afterdischarges induced by electrical stimulation of the dorsal hippocampus in mice , 1997, Psychobiology.

[28]  J. Aggleton,et al.  Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat , 1996, Behavioural Brain Research.

[29]  K O Lim,et al.  Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. , 1995, Alcoholism, clinical and experimental research.

[30]  E. Tulving,et al.  Memory beyond the hippocampus , 1997, Current Opinion in Neurobiology.

[31]  Richard S. J. Frackowiak,et al.  The role of the right hemisphere in the interpretation of figurative aspects of language. A positron emission tomography activation study. , 1994, Brain : a journal of neurology.

[32]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[33]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[34]  Lars Nyberg,et al.  Asymmetric frontal activation during episodic memory: what kind of specificity? , 1998, Trends in Cognitive Sciences.

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

[36]  A. Mayes,et al.  Human organic memory disorders , 1988 .

[37]  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.

[38]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.

[39]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[40]  A. Mayes,et al.  Rate of forgetting in amnesia: I. Recall and recognition of prose. , 1999, Journal of Experimental Psychology. Learning, Memory and Cognition.

[41]  E. Rolls A theory of hippocampal function in memory , 1996, Hippocampus.

[42]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[43]  J. Aggleton,et al.  Amnesia and recognition memory: A re-analysis of psychometric data , 1996, Neuropsychologia.

[44]  David G. Amaral,et al.  Introduction: What is where in the medial temporal lobe? , 1999, Hippocampus.

[45]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.

[46]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[47]  A R McIntosh,et al.  The neural correlates of intentional learning of verbal materials: a PET study in humans. , 1996, Brain research. Cognitive brain research.

[48]  P. Grasby,et al.  PET activation of the medial temporal lobe in learning. , 1998, Brain : a journal of neurology.

[49]  G. Glover,et al.  Level of sustained entorhinal activity at study correlates with subsequent cued‐recall performance: A functional magnetic resonance imaging study with high acquisition rate , 1999, Hippocampus.

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

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

[52]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[53]  Karl J. Friston Imaging cognitive anatomy , 1997, Trends in Cognitive Sciences.

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

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

[56]  A. Mayes,et al.  What do theories of the functional deficit(s) underlying amnesia have to explain? , 1997, Memory.

[57]  A. Anderson,et al.  Specifying the Contributions of the Human Amygdala to Emotional Memory: A Case Study , 1998 .

[58]  R. C. Honey,et al.  Hippocampal Lesions Disrupt an Associative Mismatch Process , 1998, The Journal of Neuroscience.

[59]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[61]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[62]  R. Elliott,et al.  Neural Response during Preference and Memory Judgments for Subliminally Presented Stimuli: A Functional Neuroimaging Study , 1998, The Journal of Neuroscience.

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

[64]  D. Montaldi,et al.  Dissociating novelty detection and associative encoding in the processing of complex scenes. , 1998, NeuroImage.

[65]  Alex Martin,et al.  Modulation of human medial temporal lobe activity by form, meaning, and experience , 1997, Hippocampus.

[66]  Michael Petrides,et al.  Lesions to the right parahippocampal cortex cause navigational memory deficits in humans , 1997 .

[67]  J. Gray The neuropsychology of anxiety. , 1985, Issues in mental health nursing.

[68]  G. Mangun,et al.  Successful Verbal Encoding into Episodic Memory Engages the Posterior Hippocampus: A Parametrically Analyzed Functional Magnetic Resonance Imaging Study , 1998, The Journal of Neuroscience.

[69]  P. Roland,et al.  The human entorhinal cortex participates in associative memory , 1994, Neuroreport.

[70]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

[71]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[72]  Leslie G. Ungerleider,et al.  Age-related reductions in human recognition memory due to impaired encoding. , 1995, Science.

[73]  B. Weber,et al.  Human hippocampus establishes associations in memory , 1997, Hippocampus.

[74]  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.

[75]  Alan C. Evans,et al.  A role for the hippocampal formation in implicit memory: a 3‐D PET study , 1998, Neuroreport.

[76]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[77]  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.

[78]  Amanda Parker,et al.  The von Restorff Effect in Visual Object Recognition Memory in Humans and Monkeys: The Role of Frontal/Perirhinal Interaction , 1998, Journal of Cognitive Neuroscience.

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

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

[81]  Practice related changes in the human brain during free recall of abstract designs , 1998, NeuroImage.

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

[83]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

[84]  Michael D. Rugg,et al.  Dissociation of the neural correlates of implicit and explicit memory , 1998, Nature.

[85]  A. Mayes,et al.  Encoding ability is preserved in amnesia: Evidence from a direct test of encoding , 1993, Neuropsychologia.

[86]  E. Maguire,et al.  Knowing Where Things Are: Parahippocampal Involvement in Encoding Object Locations in Virtual Large-Scale Space , 1998, Journal of Cognitive Neuroscience.

[87]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[88]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[89]  D J Wyper,et al.  Associative encoding of pictures activates the medial temporal lobes , 1998, Human brain mapping.

[90]  J. Desmond,et al.  Material‐specific lateralization of prefrontal activation during episodic encoding and retrieval , 1998, Neuroreport.

[91]  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.

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

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