Activity in human medial temporal lobe associated with encoding process in spatial working memory revealed by magnetoencephalography

Animal studies have suggested that working memory may be affected after lesions in the medial temporal lobe, although this assumption has not been corroborated by neuropsychological studies in humans. However, very recently, several functional neuroimaging studies in humans have successfully observed activation of the medial temporal lobe during working memory tasks. The main aim of this study was to investigate the contribution of the medial temporal lobe to the encoding process in spatial working memory. To address this issue we registered the neuromagnetic brain patterns of eight adult volunteers while they performed a spatial working memory task and more perceptual task using identical stimuli. After a initial phase (between 200 and 400 ms) without differences in activation, the medial temporal lobe showed a sustained activity, more evident in the right hemisphere, lasting up to 800 ms during the encoding stage of the spatial working memory task, while the activation in the perceptual task terminated earlier (∼400 ms after stimulus onset). The finding of a continued activation of the medial temporal lobe strongly suggests the contribution of this brain region to encoding operations in working memory.

[1]  J. Fuster.  Memory in the cerebral cortex , 1994 .

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

[3]  D. Gitelman,et al.  Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects , 1999, NeuroImage.

[4]  J. Sarvas.  Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[5]  C R Jack,et al.  MRI hippocampal volumes and memory function before and after temporal lobectomy , 1993, Neurology.

[6]  Edward Awh,et al.  The Role of Spatial Selective Attention in Working Memory for Locations: Evidence from Event-Related Potentials , 2000, Journal of Cognitive Neuroscience.

[7]  R. N. Davis,et al.  Levels of word processing and incidental memory: dissociable mechanisms in the temporal lobe , 2001, Neuroreport.

[8]  D. Schacter,et al.  When encoding yields remembering: insights from event-related neuroimaging. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  C. Tesche,et al.  Non-invasive detection of ongoing neuronal population activity in normal human hippocampus , 1997, Brain Research.

[10]  N. Phillips,et al.  Grouped data do not tell the whole story: individual analysis of cognitive change after temporal lobectomy. , 1995, Journal of clinical and experimental neuropsychology.

[11]  A. Saykin,et al.  Functional differentiation of medial temporal and frontal regions involved in processing novel and familiar words: an fMRI study. , 1999, Brain : a journal of neurology.

[12]  T. Cizadlo,et al.  Short-term and long-term verbal memory: a positron emission tomography study. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews Neuroscience.

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

[15]  J C Gore,et al.  Network analysis of brain activations in working memory: Behavior and age relationships , 2000, Microscopy research and technique.

[16]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[17]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. D’Esposito,et al.  Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information , 2001, Neuron.

[19]  Michael X. Cohen,et al.  Inferior Temporal, Prefrontal, and Hippocampal Contributions to Visual Working Memory Maintenance and Associative Memory Retrieval , 2004, The Journal of Neuroscience.

[20]  The dynamic processes for word and picture encoding in the human brain as revealed by magnetoencephalography , 2000, Neuroscience Letters.

[21]  P S Goldman-Rakic,et al.  Primate rhinal cortex participates in both visual recognition and working memory tasks: functional mapping with 2-DG. , 2001, Journal of neurophysiology.

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

[23]  C. Curtis,et al.  Object and spatial alternation tasks with minimal delays activate the right anterior hippocampus proper in humans , 2000, Neuroreport.

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

[25]  C. Stark,et al.  Making Memories without Trying: Medial Temporal Lobe Activity Associated with Incidental Memory Formation during Recognition , 2003, The Journal of Neuroscience.

[26]  Christopher S. Monk,et al.  Human hippocampal activation in the delayed matching- and nonmatching-to-sample memory tasks: an event-related functional MRI approach. , 2002, Behavioral neuroscience.

[27]  A. Papanicolaou,et al.  Magnetocephalography: a noninvasive alternative to the Wada procedure. , 2004, Journal of neurosurgery.

[28]  B R Postle,et al.  "What"-Then-Where" in visual working memory: an event-related fMRI study. , 1999, Journal of cognitive neuroscience.

[29]  Panagiotis G. Simos,et al.  Modulation of brain magnetic activity by different verbal learning strategies , 2003, NeuroImage.

[30]  Henrik Walter,et al.  Dissociating a Common Working Memory Network from Different Neural Substrates of Phonological and Spatial Stimulus Processing , 2002, NeuroImage.

[31]  M. D’Esposito,et al.  Temporal isolation of the neural correlates of spatial mnemonic processing with fMRI. , 1999, Brain research. Cognitive brain research.

[32]  A. Wyler,et al.  Hippocampal sclerosis and verbal encoding ability following anterior temporal lobectomy , 1996, Neuropsychologia.

[33]  J. Desmond,et al.  Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. , 2001, Brain : a journal of neurology.

[34]  C D Tesche,et al.  Non-invasive detection of neuronal population activity in human hippocampus. , 1996, Brain research. Cognitive brain research.

[35]  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.

[36]  Alan C. Evans,et al.  A cognitive activation study of memory for spatialrelationshipsfn2 fn2 Study conducted at the McConnellBrain Imaging Centre, Montreal Neurological Institute,McGill University. , 1999, Neuropsychologia.

[37]  Wilfried Lang,et al.  Left Temporal and Temporoparietal Brain Activity Depends on Depth of Word Encoding: A Magnetoencephalographic Study in Healthy Young Subjects , 2001, NeuroImage.

[38]  G Zouridakis,et al.  Magnetoencephalographic mapping of the language-specific cortex. , 1998, Journal of neurosurgery.

[39]  O. Gruber,et al.  Domain-specific distribution of working memory processes along human prefrontal and parietal cortices: a functional magnetic resonance imaging study , 2001, Neuroscience Letters.

[40]  N. Lynöe,et al.  Informed consent: study of quality of information given to participants in a clinical trial. , 1991, BMJ.

[41]  Paul J Reber,et al.  Encoding activity in the medial temporal lobe examined with anatomically constrained fMRI analysis , 2002, Hippocampus.

[42]  W. Suzuki,et al.  The Long and the Short of It Memory Signals in the Medial Temporal Lobe , 1999, Neuron.

[43]  Alberto Fernández,et al.  Is medial temporal lobe activation specific for encoding long-term memories? , 2005, NeuroImage.

[44]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

[45]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[46]  M. Greicius,et al.  Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study , 2003, Hippocampus.

[47]  Dick J. Veltman,et al.  Deep processing activates the medial temporal lobe in young but not in old adults , 2003, Neurobiology of Aging.

[48]  A. Capilla,et al.  Prefrontal brain magnetic activity: effects of memory task demands. , 2005, Neuropsychology.

[49]  A. Papanicolaou,et al.  The hippocampus and memory of verbal and pictorial material. , 2002, Learning & memory.

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

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

[52]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[53]  Alberto Fernández,et al.  Time modulated prefrontal and parietal activity during the maintenance of integrated information as revealed by magnetoencephalography. , 2004, Cerebral cortex.

[54]  G. Glover,et al.  Analysis of a distributed neural system involved in spatial information, novelty, and memory processing , 2000, Human brain mapping.

[55]  Stephen T. C. Wong,et al.  Magnetoencephalography in partial epilepsy: Clinical yield and localization accuracy , 1997, Annals of neurology.

[56]  Joshua I. Breier,et al.  Integrating sensory and motor mapping in a comprehensive MEG protocol: Clinical validity and replicability , 2004, NeuroImage.

[57]  C. Frith,et al.  Differential Activation of Right Superior Parietal Cortex and Intraparietal Sulcus by Spatial and Nonspatial Attention , 1998, NeuroImage.

[58]  J. Fletcher,et al.  Brain mechanisms for reading words and pseudowords: an integrated approach. , 2002, Cerebral cortex.

[59]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[60]  S. Salenius,et al.  Roles of attention, memory, and motor preparation in modulating human brain activity in a spatial working memory task. , 1998, Cerebral cortex.

[61]  E. Rolls,et al.  Role of long‐term synaptic modification in short‐term memory , 2001, Hippocampus.

[62]  L. Davachi,et al.  Hippocampal contributions to episodic encoding: insights from relational and item-based learning. , 2002, Journal of neurophysiology.

[63]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[64]  C. Elger,et al.  Relations Between Verbal and Nonverbal Memory Performance: Evidence of Confounding Effects Particulary in Patients with Right Temporal Lobe Epilepsy , 1995, Cortex.

[65]  Joshua R. Smith,et al.  A Comparison of Magnetoencephalography, MRI, and V‐EEG in Patients Evaluated for Epilepsy Surgery , 1999, Epilepsia.

[66]  R. Salmelin,et al.  Distinct time courses of word and context comprehension in the left temporal cortex. , 1998, Brain : a journal of neurology.

[67]  Florin Dolcos,et al.  Similarities and Differences in the Neural Correlates of Episodic Memory Retrieval and Working Memory , 2002, NeuroImage.

[68]  Mingxiong Huang,et al.  A non-invasive method for observing hippocampal function , 2003, Neuroreport.

[69]  David G. Amaral,et al.  21 – Hippocampal Formation , 1990 .

[70]  C. Stern,et al.  Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli , 2001, Hippocampus.

[71]  Christoph Baumgartner,et al.  Magnetoencephalography in presurgical epilepsy evaluation , 2002, Neurosurgical Review.

[72]  R. Rausch,et al.  Performance of Patients with Unilateral Temporal Lobectomy on Selective Reminding Procedures Using Either Related or Unrelated Words , 1990, Cortex.

[73]  G Zouridakis,et al.  Temporal course of regional brain activation associated with phonological decoding. , 1999, Journal of clinical and experimental neuropsychology.

[74]  Santiago Fernández,et al.  Spanish Language Mapping Using MEG: A Validation Study , 2002, NeuroImage.