Recollection of vivid memories after perirhinal region stimulations: synchronization in the theta range of spatially distributed brain areas

Electrical stimulation of the temporal cortex in patients with epilepsy sometimes elicits experiential phenomena such as recollection of vivid memories. The neurophysiological substrate of such phenomena is poorly understood. Furthermore, the relation between the site of stimulation and the type of memory elicited has only recently started to be investigated. We investigated these issues in patient FGA who had intracerebral electrodes stereotaxically implanted in the right temporal lobe for investigation of drug-resistant epilepsy. We report the results of electrical stimulations of the perirhinal region. Two stimulations elicited experiential phenomena consisting of visual memories that belonged to FGA's past, but which were not related to any particular episode. These visual memories consisted of objects or of details of objects. These two stimulations were contrasted with other stimulations in the same subhippocampal region. Cross-correlation analysis of the depth-EEG signals filtered in frequency sub-bands revealed that experiential phenomena occurred only when the various brain structures involved in the after-discharge were synchronized in the theta range. These structures included the perirhinal region, the hippocampus, other limbic structures as well as a primary visual area. Our results suggest that recollection of vivid memory after electric stimulation of the cortex may rely on wide networks of brain areas that transiently synchronize. These results also highlight the role of the perirhinal region in human memory. Experiential phenomena are rarely obtained after brain stimulation. Replication of these results is thus required due to the small number of observations reported.

[1]  P Gloor,et al.  Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. , 1990, Brain : a journal of neurology.

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

[3]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Halgren,et al.  Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. , 1978, Brain : a journal of neurology.

[5]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

[6]  A. Engel,et al.  Cognitive functions of gamma-band activity: memory match and utilization , 2004, Trends in Cognitive Sciences.

[7]  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.

[8]  S. Kosslyn,et al.  Neural foundations of imagery , 2001, Nature Reviews Neuroscience.

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

[10]  Alfred L. Goldberg.  Memory Mechanisms , 1964, Science.

[11]  W. Penfield,et al.  THE BRAIN'S RECORD OF AUDITORY AND VISUAL EXPERIENCE. A FINAL SUMMARY AND DISCUSSION. , 1963, Brain : a journal of neurology.

[12]  Fernando H. Lopes da Silva,et al.  Propagation of Electrical Activity: Nonlinear Associations and Time Delays between EEG Signals , 1993 .

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

[14]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[15]  Wendy A Suzuki,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cytoarchitectonic and chemoarchitectonic organization , 2003, The Journal of comparative neurology.

[16]  J. Jackson,et al.  EPILEPTIC ATTACKS WITH A WARNING OF A CRUDE SENSATION OF SMELL AND WITH THE INTELLECTUAL AURA (DREAMY STATE) IN A PATIENT WHO HAD SYMPTOMS POINTING TO GROSS ORGANIC DISEASE OF THE RIGHT TEMPORO-SPHENOIDAL LOBE , 1899 .

[17]  J. Bellanger,et al.  Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. , 2003, Brain : a journal of neurology.

[18]  E. Tulving,et al.  Episodic and declarative memory: Role of the hippocampus , 1998, Hippocampus.

[19]  A. R. Lurii︠a︡,et al.  The neuropsychology of memory , 1977 .

[20]  Joseph R. Madsen,et al.  Human theta oscillations exhibit task dependence during virtual maze navigation , 1999, Nature.

[21]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[22]  E.-J. Speckmann,et al.  Basic Mechanisms of the EEG , 1993, Brain Dynamics.

[23]  Seth J. Ramus,et al.  Dissociation between the effects of damage to perirhinal cortex and area TE. , 1999, Learning & memory.

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

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

[26]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[27]  J. Hughlings Jackson,et al.  CASE OF EPILEPSY WITH TASTING MOVEMENTS AND “DREAMY STATE”—VERY SMALL PATCH OF SOFTENING IN THE LEFT UNCINATE GYRUS , 1898 .

[28]  W. Klimesch,et al.  Theta synchronization during episodic retrieval: neural correlates of conscious awareness. , 2001, Brain research. Cognitive brain research.

[29]  H. Saunders.  Literature Review : RANDOM DATA: ANALYSIS AND MEASUREMENT PROCEDURES J. S. Bendat and A.G. Piersol Wiley-Interscience, New York, N. Y. (1971) , 1974 .

[30]  J. Fell,et al.  Rhinal–hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? , 2003, The European journal of neuroscience.

[31]  M Guye,et al.  Cortical stimulation study of the role of rhinal cortex in déjà vu and reminiscence of memories , 2004, Neurology.

[32]  E. Halgren,et al.  Anatomical origin of déjà vu and vivid 'memories' in human temporal lobe epilepsy. , 1994, Brain : a journal of neurology.

[33]  E. Halgren,et al.  Experimental phenomena evoked by human brain electrical stimulation. , 1993, Advances in neurology.

[34]  Orrin Devinsky,et al.  Electrical and Magnetic Stimulation of the Brain and Spinal Cord , 1993 .

[35]  L. Squire,et al.  Episodic memory, semantic memory, and amnesia , 1998, Hippocampus.

[36]  A D Baddeley,et al.  The autobiographical memory interview: a new assessment of autobiographical and personal semantic memory in amnesic patients. , 1989, Journal of clinical and experimental neuropsychology.

[37]  J. Kelso,et al.  Cortical coordination dynamics and cognition , 2001, Trends in Cognitive Sciences.

[38]  P. Gloor,et al.  The role of the limbic system in experiential phenomena of temporal lobe epilepsy , 1982, Annals of neurology.

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

[40]  B. Richmond,et al.  Role of perirhinal cortex in object perception, memory, and associations , 2001, Current Opinion in Neurobiology.