Remote Effects of Hippocampal Sclerosis on Effective Connectivity during Working Memory Encoding: A Case of Connectional Diaschisis?

Accumulating evidence suggests a role for the medial temporal lobe (MTL) in working memory (WM). However, little is known concerning its functional interactions with other cortical regions in the distributed neural network subserving WM. To reveal these, we availed of subjects with MTL damage and characterized changes in effective connectivity while subjects engaged in WM task. Specifically, we compared dynamic causal models, extracted from magnetoencephalographic recordings during verbal WM encoding, in temporal lobe epilepsy patients (with left hippocampal sclerosis) and controls. Bayesian model comparison indicated that the best model (across subjects) evidenced bilateral, forward, and backward connections, coupling inferior temporal cortex (ITC), inferior frontal cortex (IFC), and MTL. MTL damage weakened backward connections from left MTL to left ITC, a decrease accompanied by strengthening of (bidirectional) connections between IFC and MTL in the contralesional hemisphere. These findings provide novel evidence concerning functional interactions between nodes of this fundamental cognitive network and sheds light on how these interactions are modified as a result of focal damage to MTL. The findings highlight that a reduced (top-down) influence of the MTL on ipsilateral language regions is accompanied by enhanced reciprocal coupling in the undamaged hemisphere providing a first demonstration of “connectional diaschisis.”

[1]  U. Noppeney,et al.  Distinct Functional Contributions of Primary Sensory and Association Areas to Audiovisual Integration in Object Categorization , 2010, The Journal of Neuroscience.

[2]  Josemir W Sander,et al.  Effects of topiramate on cognitive function , 2000, Journal of neurology, neurosurgery, and psychiatry.

[3]  Karl J. Friston,et al.  A neural mass model for MEG/EEG: coupling and neuronal dynamics , 2003, NeuroImage.

[4]  S. Bressler,et al.  Large-scale brain networks in cognition: emerging methods and principles , 2010, Trends in Cognitive Sciences.

[5]  John Jonides,et al.  Neural correlates of access to short-term memory , 2008, Proceedings of the National Academy of Sciences.

[6]  Nacim Betrouni,et al.  Attention impairment in temporal lobe epilepsy: A neurophysiological approach via analysis of the P300 wave , 2009, Human brain mapping.

[7]  P. Hofman,et al.  Cognitive fMRI and neuropsychological assessment in patients with secondarily generalized seizures , 2008, Clinical Neurology and Neurosurgery.

[8]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

[9]  Fernando Maestú,et al.  Modulation of medial temporal lobe activity in epilepsy patients with hippocampal sclerosis during verbal working memory , 2009, Journal of the International Neuropsychological Society.

[10]  Klaas E. Stephan,et al.  Dynamic causal modelling: A critical review of the biophysical and statistical foundations , 2011, NeuroImage.

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

[12]  M. D’Esposito,et al.  Directing the mind's eye: prefrontal, inferior and medial temporal mechanisms for visual working memory , 2005, Current Opinion in Neurobiology.

[13]  K. Meador Cognitive and memory effects of the new antiepileptic drugs , 2006, Epilepsy Research.

[14]  Michael W Weiner,et al.  Different structural correlates for verbal memory impairment in temporal lobe epilepsy with and without mesial temporal lobe sclerosis , 2012, Human brain mapping.

[15]  Maria Paola Canevini,et al.  Relationship between adverse effects of antiepileptic drugs, number of coprescribed drugs, and drug load in a large cohort of consecutive patients with drug‐refractory epilepsy , 2010, Epilepsia.

[16]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[17]  J. Duncan,et al.  Cognitive consequences of childhood-onset temporal lobe epilepsy across the adult lifespan , 2010, Neurology.

[18]  E. Mervaala,et al.  Lateralization of Event‐Related Potentials During Discontinuation of Antiepileptic Medication , 1995, Epilepsia.

[19]  J. Régis,et al.  Enhanced EEG functional connectivity in mesial temporal lobe epilepsy , 2008, Epilepsy Research.

[20]  Theo G. M. van Erp,et al.  Hippocampal activations during encoding and retrieval in a verbal working memory paradigm , 2005, NeuroImage.

[21]  S. González Índices de interés psicolingüístico de 1917 palabras castellanas , 1996 .

[22]  J B Poline,et al.  Episodic memory in left temporal lobe epilepsy: a functional MRI study. , 2000, Brain : a journal of neurology.

[23]  Nikolai Axmacher,et al.  Interactions between Medial Temporal Lobe, Prefrontal Cortex, and Inferior Temporal Regions during Visual Working Memory: A Combined Intracranial EEG and Functional Magnetic Resonance Imaging Study , 2008, The Journal of Neuroscience.

[24]  Morris Moscovitch,et al.  Consequences of hippocampal damage across the autobiographical memory network in left temporal lobe epilepsy. , 2007, Brain : a journal of neurology.

[25]  J. Malagón-Valdéz [Cognitive effects of antiepileptic drugs]. , 2003, Revista de neurologia.

[26]  David L. Sheinberg,et al.  Neural Dynamics in Inferior Temporal Cortex during a Visual Working Memory Task , 2009, The Journal of Neuroscience.

[27]  J. Cramer,et al.  Cognition across the lifespan: Antiepileptic drugs, epilepsy, or both? , 2010, Epilepsy & Behavior.

[28]  D. Velis,et al.  Long-Term Effects of Temporal Lobe Epilepsy on Local Neural Networks: A Graph Theoretical Analysis of Corticography Recordings , 2009, PloS one.

[29]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

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

[31]  O. Bertrand,et al.  Neural correlates of consolidation in working memory , 2007, Human brain mapping.

[32]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[33]  Gregory G. Brown,et al.  Methodological and conceptual issues in functional magnetic resonance imaging: applications to schizophrenia research. , 2006, Annual review of clinical psychology.

[34]  Krista E. Garver,et al.  Material-specific lateralization of working memory in the medial temporal lobe , 2009, Neuropsychologia.

[35]  Viktor K. Jirsa,et al.  Handbook of Brain Connectivity , 2007 .

[36]  Katherine Carpenter,et al.  Functional and structural changes in the memory network associated with left temporal lobe epilepsy , 2009, Human brain mapping.

[37]  John S. Duncan,et al.  Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus , 2004, NeuroImage.

[38]  Anjan Chatterjee,et al.  Visual Working Memory Is Impaired when the Medial Temporal Lobe Is Damaged , 2006, Journal of Cognitive Neuroscience.

[39]  Karl J. Friston,et al.  Modulation of Perception and Brain Activity by Predictable Trajectories of Facial Expressions , 2009, Cerebral cortex.

[40]  R. Buckner,et al.  Changing frontal contributions to memory before and after medial temporal lobectomy. , 2006, Cerebral cortex.

[41]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses in EEG/MEG with lead field parameterization , 2006, NeuroImage.

[42]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[43]  Lila Davachi,et al.  Are Representations in Working Memory Distinct From Representations in Long-Term Memory? , 2010, Psychological science.

[44]  C. E. Polkey,et al.  Hippocampal Involvement in Spatial and Working Memory: A Structural MRI Analysis of Patients with Unilateral Mesial Temporal Lobe Sclerosis , 1999, Brain and Cognition.

[45]  Michael X. Cohen,et al.  Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe , 2007, The Journal of Neuroscience.

[46]  Michel Baulac,et al.  Effect of Unilateral Temporal Lobe Resection on Short‐Term Memory for Auditory Object and Sound Location , 2003, Annals of the New York Academy of Sciences.

[47]  Karl J. Friston,et al.  Dynamic causal modelling of evoked potentials: A reproducibility study , 2007, NeuroImage.

[48]  M. Mesulam,et al.  Shifts of Effective Connectivity within a Language Network during Rhyming and Spelling , 2005, The Journal of Neuroscience.

[49]  D. Ruchkin,et al.  Mesial temporal spikes interfere with working memory , 1997, Neurology.

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

[51]  Karl J. Friston,et al.  Dynamic Diaschisis: Anatomically Remote and Context-Sensitive Human Brain Lesions , 2001, Journal of Cognitive Neuroscience.

[52]  Karl J. Friston Causal Modelling and Brain Connectivity in Functional Magnetic Resonance Imaging , 2009, PLoS biology.

[53]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[54]  Craig J. Brozinsky,et al.  Functional connectivity with the hippocampus during successful memory formation , 2005, Hippocampus.

[55]  K. Amunts,et al.  Effective connectivity of the left BA 44, BA 45, and inferior temporal gyrus during lexical and phonological decisions identified with DCM , 2009, Human brain mapping.

[56]  Karl Magnus Petersson,et al.  Interaction between a verbal working memory network and the medial temporal lobe , 2006, NeuroImage.

[57]  Olivier David,et al.  Dynamic Causal Modelling and physiological confounds: A functional MRI study of vagus nerve stimulation , 2010, NeuroImage.

[58]  A. Mechelli,et al.  Functional integration between the posterior hippocampus and prefrontal cortex is impaired in both first episode schizophrenia and the at risk mental state. , 2009, Brain : a journal of neurology.

[59]  Peter Zeidman,et al.  Identifying Abnormal Connectivity in Patients Using Dynamic Causal Modeling of fMRI Responses , 2010, Front. Syst. Neurosci..

[60]  Olivier David,et al.  Dynamic causal models and autopoietic systems. , 2007, Biological research.

[61]  P. Chauvel,et al.  Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms , 2009, Human brain mapping.

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

[63]  Huafu Chen,et al.  Altered Functional Connectivity and Small-World in Mesial Temporal Lobe Epilepsy , 2010, PloS one.

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

[65]  F. Bartolomei,et al.  Imaging structural and functional connectivity: towards a unified definition of human brain organization? , 2008, Current opinion in neurology.

[66]  S. Berkovic,et al.  Lateralization of verbal memory and unilateral hippocampal sclerosis: evidence of task-specific effects. , 1993, Journal of clinical and experimental neuropsychology.

[67]  Karl J. Friston,et al.  Canonical Source Reconstruction for MEG , 2007, Comput. Intell. Neurosci..

[68]  Karine Lebreton,et al.  Is Neocortical–Hippocampal Connectivity a Better Predictor of Subsequent Recollection than Local Increases in Hippocampal Activity? New Insights on the Role of Priming , 2011, Journal of Cognitive Neuroscience.

[69]  Yufeng Zang,et al.  Abnormal Functional Connectivity of Hippocampus During Episodic Memory Retrieval Processing Network in Amnestic Mild Cognitive Impairment , 2009, Biological Psychiatry.

[70]  Karl J. Friston,et al.  Dynamic representations and generative models of brain function , 2001, Brain Research Bulletin.

[71]  Karl J. Friston,et al.  Two distinct neural mechanisms for category-selective responses. , 2006, Cerebral cortex.

[72]  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.

[73]  P. Pietrini,et al.  Altered brain functional connectivity and impaired short-term memory in Alzheimer's disease. , 2001, Brain : a journal of neurology.

[74]  David Corina,et al.  The roles of human lateral temporal cortical neuronal activity in recent verbal memory encoding. , 2009, Cerebral cortex.

[75]  I. Olson,et al.  The medial temporal lobe and visual working memory: Comparisons across tasks, delays, and visual similarity , 2008, Cognitive, affective & behavioral neuroscience.

[76]  Y. Miyashita,et al.  Formation of mnemonic neuronal responses to visual paired associates in inferotemporal cortex is impaired by perirhinal and entorhinal lesions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[77]  J. Fuster Inferotemporal units in selective visual attention and short-term memory. , 1990, Journal of neurophysiology.

[78]  A R McIntosh,et al.  Frontotemporal interactions in face encoding and recognition. , 1999, Brain research. Cognitive brain research.

[79]  Andreas Schulze-Bonhage,et al.  Hippocampal functional connectivity reflects verbal episodic memory network integrity , 2007, Neuroreport.

[80]  P. Hoffman,et al.  Selective short-term memory deficits arise from impaired domain-general semantic control mechanisms. , 2009, Journal of experimental psychology. Learning, memory, and cognition.

[81]  Andy C. H. Lee,et al.  Differentiating the Roles of the Hippocampus and Perirhinal Cortex in Processes beyond Long-Term Declarative Memory: A Double Dissociation in Dementia , 2006, The Journal of Neuroscience.

[82]  Karl J. Friston,et al.  Repetition suppression and plasticity in the human brain , 2009, NeuroImage.

[83]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

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

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

[86]  E. Bilevicius,et al.  Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI , 2010, BMC Neuroscience.

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

[88]  Angela D. Friederici,et al.  Lateral Inferotemporal Cortex Maintains ConceptualSemantic Representations in Verbal Working Memory , 2007, Journal of Cognitive Neuroscience.

[89]  Karl J. Friston,et al.  Models of Effective Connectivity in Neural Systems , 2007 .

[90]  Ho-Won Lee,et al.  Comparison of Cognitive Effects of Lamotrigine and Oxcarbazepine in Epilepsy Patients , 2007, Journal of clinical neurology.

[91]  A R McIntosh,et al.  Neural correlates of semantic associative encoding in episodic memory. , 2000, Brain research. Cognitive brain research.

[92]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[93]  John S Duncan,et al.  Reorganization of Verbal and Nonverbal Memory in Temporal Lobe Epilepsy Due to Unilateral Hippocampal Sclerosis , 2007, Epilepsia.

[94]  Karl J. Friston,et al.  Topological inference for EEG and MEG , 2010, 1011.2901.

[95]  Andreas Schulze-Bonhage,et al.  Remote effects of hippocampal damage on default network connectivity in the human brain , 2009, Journal of Neurology.

[96]  J. Rich,et al.  Deaths of detainees in the custody of US forces in Iraq and Afghanistan from 2002 to 2005. , 2006, MedGenMed : Medscape general medicine.

[97]  Andrew A Fingelkurts,et al.  Enhancement of GABA‐related signalling is associated with increase of functional connectivity in human cortex , 2004, Human brain mapping.

[98]  Karl J. Friston,et al.  Dynamic Causal Modeling of the Response to Frequency Deviants , 2009, Journal of neurophysiology.

[99]  Maria Thom,et al.  Quantitative post-mortem study of the hippocampus in chronic epilepsy: seizures do not inevitably cause neuronal loss. , 2005, Brain : a journal of neurology.

[100]  Hitten P. Zaveri,et al.  Background intracranial EEG spectral changes with anti-epileptic drug taper , 2010, Clinical Neurophysiology.

[101]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

[102]  M. Saling,et al.  Verbal memory in mesial temporal lobe epilepsy: beyond material specificity. , 2009, Brain : a journal of neurology.

[103]  J. Cramer,et al.  Effect of valproate on cognitive functioning. Comparison with carbamazepine. The Department of Veterans Affairs Epilepsy Cooperative Study 264 Group. , 1996, Archives of neurology.

[104]  Ryu-ichiro Hashimoto,et al.  An fMRI study of functional abnormalities in the verbal working memory system and the relationship to clinical symptoms in chronic schizophrenia. , 2010, Cerebral cortex.

[105]  John S. Duncan,et al.  Tractography of the parahippocampal gyrus and material specific memory impairment in unilateral temporal lobe epilepsy , 2007, NeuroImage.

[106]  Giuliano Avanzini,et al.  Semantic memory in partial epilepsy: verbal and non-verbal deficits and neuroanatomical relationships , 2005, Neuropsychologia.

[107]  Adam Gazzaley,et al.  Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. , 2008, Cerebral cortex.

[108]  J. Arends,et al.  Randomized Double‐blind Parallel‐group Study Comparing Cognitive Effects of a Low‐dose Lamotrigine with Valproate and Placebo in Healthy Volunteers , 2002, Epilepsia.

[109]  Karl J. Friston,et al.  Evoked brain responses are generated by feedback loops , 2007, Proceedings of the National Academy of Sciences.

[110]  K. Meador,et al.  Neuropsychological and neurophysiologic effects of carbamazepine and levetiracetam , 2007, Neurology.

[111]  Cheryl L Grady,et al.  Age‐related differences in the functional connectivity of the hippocampus during memory encoding , 2003, Hippocampus.

[112]  A M Owen,et al.  Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. , 1996, Brain : a journal of neurology.

[113]  Yuping Wang,et al.  Antiepileptic Drugs and the Significance of Event-Related Potentials , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[114]  Nicole David,et al.  Being with virtual others: Studying social cognition in temporal lobe epilepsy , 2007, Epilepsy & Behavior.

[115]  M. Hasselmo,et al.  Greater working memory load results in greater medial temporal activity at retrieval. , 2009, Cerebral cortex.

[116]  R. Kessels,et al.  Spatial and non-spatial contextual working memory in patients with diencephalic or hippocampal dysfunction , 2007, Brain Research.

[117]  Paul Allen,et al.  Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations , 2007, Human brain mapping.

[118]  Karl J. Friston,et al.  Dynamic causal modeling of evoked responses in EEG and MEG , 2006, NeuroImage.

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

[120]  C. Gualtieri,et al.  Comparative neurocognitive effects of 5 psychotropic anticonvulsants and lithium. , 2006, MedGenMed : Medscape general medicine.

[121]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.