The subiculum and its role in focal epileptic disorders

Abstract The subicular complex (hereafter referred as subiculum), which is reciprocally connected with the hippocampus and rhinal cortices, exerts a major control on hippocampal outputs. Over the last three decades, several studies have revealed that the subiculum plays a pivotal role in learning and memory but also in pathological conditions such as mesial temporal lobe epilepsy (MTLE). Indeed, subicular networks actively contribute to seizure generation and this structure is relatively spared from the cell loss encountered in this focal epileptic disorder. In this review, we will address: (i) the functional properties of subicular principal cells under normal and pathological conditions; (ii) the subiculum role in sustaining seizures in in vivo models of MTLE and in in vitro models of epileptiform synchronization; (iii) its presumptive role in human MTLE; and (iv) evidence underscoring the relationship between subiculum and antiepileptic drug effects. The studies reviewed here reinforce the view that the subiculum represents a limbic area with relevant, as yet unexplored, roles in focal epilepsy.

[1]  G. Maccaferri,et al.  The intrinsic cell type‐specific excitatory connectivity of the developing mouse subiculum is sufficient to generate synchronous epileptiform activity , 2020, The Journal of physiology.

[2]  G. Torromino,et al.  Offline ventral subiculum-ventral striatum serial communication is required for spatial memory consolidation , 2019, Nature Communications.

[3]  S. Duan,et al.  Subicular pyramidal neurons gate drug resistance in temporal lobe epilepsy , 2019, Annals of neurology.

[4]  Kevin G. Johnston,et al.  CA1-Projecting Subiculum Neurons Facilitate Object-Place Learning , 2019, Nature Neuroscience.

[5]  J. Mellor,et al.  Neuromodulation of hippocampal long-term synaptic plasticity , 2019, Current Opinion in Neurobiology.

[6]  P. Hof,et al.  Subfield-specific tractography of the hippocampus in epilepsy patients at 7 Tesla , 2018, Seizure.

[7]  Mark S. Cembrowski,et al.  The subiculum is a patchwork of discrete subregions , 2018, eLife.

[8]  M. Avoli,et al.  Carbachol-Induced theta-like oscillations in the rodent brain limbic system: Underlying mechanisms and significance , 2018, Neuroscience & Biobehavioral Reviews.

[9]  M. Avoli,et al.  Phase-amplitude coupling and epileptogenesis in an animal model of mesial temporal lobe epilepsy , 2018, Neurobiology of Disease.

[10]  Michael Brecht,et al.  Burst Firing and Spatial Coding in Subicular Principal Cells , 2018, The Journal of Neuroscience.

[11]  M. Avoli,et al.  KCC2, epileptiform synchronization, and epileptic disorders , 2017, Progress in Neurobiology.

[12]  Y. Izumi,et al.  The role of T‐type calcium channels in the subiculum: to burst or not to burst? , 2017, The Journal of physiology.

[13]  M. Avoli,et al.  Time-dependent evolution of seizures in a model of mesial temporal lobe epilepsy , 2017, Neurobiology of Disease.

[14]  Fabrice Wendling,et al.  Update on the mechanisms and roles of high‐frequency oscillations in seizures and epileptic disorders , 2017, Epilepsia.

[15]  Yi Wang,et al.  Depolarized GABAergic Signaling in Subicular Microcircuits Mediates Generalized Seizure in Temporal Lobe Epilepsy , 2017, Neuron.

[16]  M. Avoli,et al.  Carbachol-induced network oscillations in an in vitro limbic system brain slice , 2017, Neuroscience.

[17]  Anton Chizhov,et al.  Reduced Efficacy of the KCC2 Cotransporter Promotes Epileptic Oscillations in a Subiculum Network Model , 2016, The Journal of Neuroscience.

[18]  Antal Berényi,et al.  Spatial coding and physiological properties of hippocampal neurons in the Cornu Ammonis subregions , 2016, Hippocampus.

[19]  K. Moxon,et al.  Role of CA3 theta-modulated interneurons during the transition to spontaneous seizures , 2016, Experimental Neurology.

[20]  B. Roth DREADDs for Neuroscientists , 2016, Neuron.

[21]  Yangfan Peng,et al.  Functional Diversity of Subicular Principal Cells during Hippocampal Ripples , 2015, The Journal of Neuroscience.

[22]  G. Buzsáki Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning , 2015, Hippocampus.

[23]  M. Avoli,et al.  Lacosamide modulates interictal spiking and high-frequency oscillations in a model of mesial temporal lobe epilepsy , 2015, Epilepsy Research.

[24]  Antoine Adamantidis,et al.  Parvalbumin Interneurons of Hippocampus Tune Population Activity at Theta Frequency , 2015, Neuron.

[25]  S. Fujita,et al.  Unit Activity of Hippocampal Interneurons before Spontaneous Seizures in an Animal Model of Temporal Lobe Epilepsy , 2015, The Journal of Neuroscience.

[26]  Richard Miles,et al.  Different mechanisms of ripple‐like oscillations in the human epileptic subiculum , 2015, Annals of neurology.

[27]  M. Avoli,et al.  The anti-ictogenic effects of levetiracetam are mirrored by interictal spiking and high-frequency oscillation changes in a model of temporal lobe epilepsy , 2015, Seizure.

[28]  S. Fujita,et al.  Preictal Activity of Subicular, CA1, and Dentate Gyrus Principal Neurons in the Dorsal Hippocampus before Spontaneous Seizures in a Rat Model of Temporal Lobe Epilepsy , 2014, The Journal of Neuroscience.

[29]  J. A. Payne,et al.  Cation-chloride cotransporters in neuronal development, plasticity and disease , 2014, Nature Reviews Neuroscience.

[30]  E. Lein,et al.  Functional organization of the hippocampal longitudinal axis , 2014, Nature Reviews Neuroscience.

[31]  Chantal E. Stern,et al.  Theta rhythm and the encoding and retrieval of space and time , 2014, NeuroImage.

[32]  R. Delorenzo,et al.  Mechanisms of Levetiracetam in the Control of Status Epilepticus and Epilepsy , 2014, Front. Neurol..

[33]  Song-Lin Ding,et al.  Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent , 2013, The Journal of comparative neurology.

[34]  Massimo Avoli,et al.  The kainic acid model of temporal lobe epilepsy , 2013, Neuroscience & Biobehavioral Reviews.

[35]  K. Moxon,et al.  Neuronal synchrony and the transition to spontaneous seizures , 2013, Experimental Neurology.

[36]  T. Hori,et al.  Surgical pathology of epilepsy‐associated non‐neoplastic cerebral lesions: A brief introduction with special reference to hippocampal sclerosis and focal cortical dysplasia , 2013, Neuropathology : official journal of the Japanese Society of Neuropathology.

[37]  Mark R. Bower,et al.  Do Seizures in the Pilocarpine Model Start in the Hippocampal Formation? , 2014, Epilepsy currents.

[38]  P. Foerch,et al.  Comparative study of lacosamide and classical sodium channel blocking antiepileptic drugs on sodium channel slow inactivation , 2013, Journal of neuroscience research.

[39]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[40]  Gabriella Panuccio,et al.  Cell Type-Specific Properties of Subicular GABAergic Currents Shape Hippocampal Output Firing Mode , 2012, PloS one.

[41]  Yi Wang,et al.  Wide therapeutic time-window of low-frequency stimulation at the subiculum for temporal lobe epilepsy treatment in rats , 2012, Neurobiology of Disease.

[42]  Jean Gotman,et al.  Two Seizure-Onset Types Reveal Specific Patterns of High-Frequency Oscillations in a Model of Temporal Lobe Epilepsy , 2012, The Journal of Neuroscience.

[43]  Fabrice Wendling,et al.  Mechanisms of physiological and epileptic HFO generation , 2012, Progress in Neurobiology.

[44]  N. Spruston,et al.  Target‐specific output patterns are predicted by the distribution of regular‐spiking and bursting pyramidal neurons in the subiculum , 2012, Hippocampus.

[45]  R. Conwit,et al.  RAMPART (Rapid Anticonvulsant Medication Prior to Arrival Trial): A double‐blind randomized clinical trial of the efficacy of intramuscular midazolam versus intravenous lorazepam in the prehospital treatment of status epilepticus by paramedics , 2011, Epilepsia.

[46]  R. Miles,et al.  Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy , 2011, Nature Neuroscience.

[47]  M. Avoli,et al.  Involvement of inward rectifier and M-type currents in carbachol-induced epileptiform synchronization , 2011, Neuropharmacology.

[48]  Javier DeFelipe,et al.  A Stereological Study of Synapse Number in the Epileptic Human Hippocampus , 2011, Front. Neuroanat..

[49]  Farshad Kheiri,et al.  Further evidence that pathologic high‐frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus , 2011, Epilepsia.

[50]  Guglielmo Foffani,et al.  Emergent Dynamics of Fast Ripples in the Epileptic Hippocampus , 2010, The Journal of Neuroscience.

[51]  M. D'Antuono,et al.  In vitro ictogenesis and parahippocampal networks in a rodent model of temporal lobe epilepsy , 2010, Neurobiology of Disease.

[52]  Noelia Montejo,et al.  Stability of subicular place fields across multiple light and dark transitions , 2010, The European journal of neuroscience.

[53]  H. Eichenbaum,et al.  Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. , 2010, Journal of neurophysiology.

[54]  N. Burgess,et al.  Brain oscillations and memory , 2010, Current Opinion in Neurobiology.

[55]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[56]  M. Rogawski,et al.  Topiramate Reduces Excitability in the Basolateral Amygdala by Selectively Inhibiting GluK1 (GluR5) Kainate Receptors on Interneurons and Positively Modulating GABAA Receptors on Principal Neurons , 2009, Journal of Pharmacology and Experimental Therapeutics.

[57]  E. Nestler Transcriptional mechanisms of addiction: role of ΔFosB , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  R. Miles,et al.  Epileptiform activities in slices of hippocampus from mice after intra‐hippocampal injection of kainic acid , 2008, The Journal of physiology.

[59]  Giuseppe Biagini,et al.  The pilocarpine model of temporal lobe epilepsy , 2008, Journal of Neuroscience Methods.

[60]  Otto W Witte,et al.  Loss of GABAergic neurons in the subiculum and its functional implications in temporal lobe epilepsy. , 2008, Brain : a journal of neurology.

[61]  D. Schmitz,et al.  Two different forms of long‐term potentiation at CA1–subiculum synapses , 2008, The Journal of physiology.

[62]  E. Halgren,et al.  Properties of in vivo interictal spike generation in the human subiculum. , 2008, Brain : a journal of neurology.

[63]  N. Spruston,et al.  Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus , 2008, The Journal of comparative neurology.

[64]  G. Lees,et al.  The Investigational Anticonvulsant Lacosamide Selectively Enhances Slow Inactivation of Voltage-Gated Sodium Channels , 2008, Molecular Pharmacology.

[65]  R. Miles,et al.  Perturbed Chloride Homeostasis and GABAergic Signaling in Human Temporal Lobe Epilepsy , 2007, The Journal of Neuroscience.

[66]  M. Avoli,et al.  Antiepileptic drugs and muscarinic receptor-dependent excitation in the rat subiculum , 2007, Neuropharmacology.

[67]  P. E. Sharp Subicular place cells generate the same “map” for different environments: Comparison with hippocampal cells , 2006, Behavioural Brain Research.

[68]  L. M. Prida,et al.  Functional features of the rat subicular microcircuits studied in vitro , 2006, Behavioural Brain Research.

[69]  Menno P. Witter,et al.  Connections of the subiculum of the rat: Topography in relation to columnar and laminar organization , 2006, Behavioural Brain Research.

[70]  M. Avoli,et al.  Subiculum network excitability is increased in a rodent model of temporal lobe epilepsy , 2006, Hippocampus.

[71]  R. Llinás,et al.  Bursting of thalamic neurons and states of vigilance. , 2006, Journal of neurophysiology.

[72]  J. Cross Neurocutaneous Syndromes and Epilepsy—Issues in Diagnosis and Management , 2005, Epilepsia.

[73]  Jozsef Csicsvari,et al.  Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations , 2005, The Journal of Neuroscience.

[74]  Shane O'Mara,et al.  The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us , 2005, Journal of anatomy.

[75]  Massimo Avoli,et al.  Rat subicular networks gate hippocampal output activity in an in vitro model of limbic seizures , 2005, The Journal of physiology.

[76]  Christian Wozny,et al.  The Subiculum: A Potential Site of Ictogenesis in Human Temporal Lobe Epilepsy , 2005, Epilepsia.

[77]  Carl E Stafstrom,et al.  The Role of the Subiculum in Epilepsy and Epileptogenesis , 2005, Epilepsy currents.

[78]  N. Spruston,et al.  Output-Mode Transitions Are Controlled by Prolonged Inactivation of Sodium Channels in Pyramidal Neurons of Subiculum , 2005, PLoS biology.

[79]  Christian Wozny,et al.  Cellular and network properties of the subiculum in the pilocarpine model of temporal lobe epilepsy , 2005, The Journal of comparative neurology.

[80]  K. Nocka,et al.  The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[81]  M. Rogawski,et al.  Topiramate selectively protects against seizures induced by ATPA, a GluR5 kainate receptor agonist , 2004, Neuropharmacology.

[82]  Govert Hoogland,et al.  Persistent sodium current in subicular neurons isolated from patients with temporal lobe epilepsy , 2004, The European journal of neuroscience.

[83]  N. Spruston,et al.  Psychostimulant-Induced Plasticity of Intrinsic Neuronal Excitability in Ventral Subiculum , 2003, The Journal of Neuroscience.

[84]  J. Noebels,et al.  Topiramate alters excitatory synaptic transmission in mouse hippocampus , 2003, Epilepsy Research.

[85]  J. Behr,et al.  Comment on "On the Origin of Interictal Activity in Human Temporal Lobe Epilepsy in Vitro" , 2003, Science.

[86]  M. Brodie,et al.  Topiramate and Lamotrigine Pharmacokinetics during Repetitive Monotherapy and Combination Therapy in Epilepsy Patients , 2003, Epilepsia.

[87]  L. Prida,et al.  Control of bursting by local inhibition in the rat subiculum in vitro , 2003 .

[88]  Juha Voipio,et al.  Cation–chloride co-transporters in neuronal communication, development and trauma , 2003, Trends in Neurosciences.

[89]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[90]  R. Miles,et al.  On the Origin of Interictal Activity in Human Temporal Lobe Epilepsy in Vitro , 2002, Science.

[91]  Itzhak Fried,et al.  Sleep States Differentiate Single Neuron Activity Recorded from Human Epileptic Hippocampus, Entorhinal Cortex, and Subiculum , 2002, The Journal of Neuroscience.

[92]  M. A. Pozo,et al.  The effect of different morphological sampling criteria on the fraction of bursting cells recorded in the rat subiculum in vitro , 2002, Neuroscience Letters.

[93]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[94]  M. Avoli,et al.  Network and intrinsic contributions to carbachol-induced oscillations in the rat subiculum. , 2001, Journal of neurophysiology.

[95]  C. Baumgartner,et al.  Plasticity of Y1 and Y2 Receptors and Neuropeptide Y Fibers in Patients with Temporal Lobe Epilepsy , 2001, The Journal of Neuroscience.

[96]  M. Witter,et al.  Intrinsic connectivity of the rat subiculum: I. Dendritic morphology and patterns of axonal arborization by pyramidal neurons , 2001, The Journal of comparative neurology.

[97]  M. Stewart,et al.  Intrinsic connectivity of the rat subiculum: II. Properties of synchronous spontaneous activity and a demonstration of multiple generator regions , 2001, The Journal of comparative neurology.

[98]  S. O’Mara,et al.  The subiculum: a review of form, physiology and function , 2001, Progress in Neurobiology.

[99]  N. Spruston,et al.  Action Potential Bursting in Subicular Pyramidal Neurons Is Driven by a Calcium Tail Current , 2001, The Journal of Neuroscience.

[100]  N Spruston,et al.  Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus. , 2000, Journal of neurophysiology.

[101]  M. de Curtis,et al.  Evidence for Spatial Modules Mediated by Temporal Synchronization of Carbachol-Induced Gamma Rhythm in Medial Entorhinal Cortex , 2000, The Journal of Neuroscience.

[102]  T. A. Morris,et al.  Chronic DeltaFosB expression and increased AP-1 transcription factor binding are associated with the long term plasticity changes in epilepsy. , 2000, Brain research. Molecular brain research.

[103]  M. Witter,et al.  Anatomical Organization of the Parahippocampal‐Hippocampal Network , 2000, Annals of the New York Academy of Sciences.

[104]  D. Sanes,et al.  Afferent Regulation of Inhibitory Synaptic Transmission in the Developing Auditory Midbrain , 2000, The Journal of Neuroscience.

[105]  M. Avoli,et al.  Topiramate depresses carbachol‐induced plateau potentials in subicular bursting cells , 2000, Neuroreport.

[106]  H. White,et al.  Topiramate Modulates GABA‐Evoked Currents in Murine Cortical Neurons by a Nonbenzodiazepine Mechanism , 2000, Epilepsia.

[107]  M. Avoli,et al.  Muscarinic receptor activation induces depolarizing plateau potentials in bursting neurons of the rat subiculum. , 1999, Journal of neurophysiology.

[108]  J. A. Payne,et al.  The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation , 1999, Nature.

[109]  S. Moshé,et al.  Hippocampal sclerosis revisited , 1998, Brain and Development.

[110]  M. Avoli,et al.  Multiple actions of the novel anticonvulsant drug topiramate in the rat subiculum in vitro , 1998, Brain Research.

[111]  E J Speckmann,et al.  Spontaneous sharp waves in human neocortical slices excised from epileptic patients. , 1998, Brain : a journal of neurology.

[112]  M. Witter,et al.  Subicular efferents are organized mostly as parallel projections: A double‐labeling, retrograde‐tracing study in the rat , 1998, The Journal of comparative neurology.

[113]  O. Devinsky The Temporal Lobe and Limbic System , 1998 .

[114]  M. Avoli,et al.  CA3-Driven Hippocampal-Entorhinal Loop Controls Rather than Sustains In Vitro Limbic Seizures , 1997, The Journal of Neuroscience.

[115]  J. Kauer,et al.  Properties of carbachol-induced oscillatory activity in rat hippocampus. , 1997, Journal of neurophysiology.

[116]  K. Kaila,et al.  Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. , 1997, Journal of neurophysiology.

[117]  S. Brown,et al.  Topiramate enhances GABA-mediated chloride flux and GABA-evoked chloride currents in murine brain neurons and increases seizure threshold , 1997, Epilepsy Research.

[118]  M. Avoli,et al.  Topiramate attenuates voltage-gated sodium currents in rat cerebellar granule cells , 1997, Neuroscience Letters.

[119]  M. Avoli,et al.  Repetitive firing and oscillatory activity of pyramidal-like bursting neurons in the rat subiculum , 1997, Experimental Brain Research.

[120]  S. Totterdell,et al.  Morphology and distribution of electrophysiologically defined classes of pyramidal and nonpyramidal neurons in rat ventral subiculum in vitro , 1997, The Journal of comparative neurology.

[121]  A. Alonso,et al.  Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. , 1997, Journal of neurophysiology.

[122]  A. Alonso,et al.  Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. , 1997, Journal of neurophysiology.

[123]  J. Lisman Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

[124]  Jerome Engel,et al.  Introduction to temporal lobe epilepsy , 1996, Epilepsy Research.

[125]  D. D. Fraser,et al.  Cholinergic-Dependent Plateau Potential in Hippocampal CA1 Pyramidal Neurons , 1996, The Journal of Neuroscience.

[126]  A Lücke,et al.  Synchronous GABA-Mediated Potentials and Epileptiform Discharges in the Rat Limbic System In Vitro , 1996, The Journal of Neuroscience.

[127]  J. Gilman Lamotrigine: an Anhepileptic Agent for the Treatment of Partial Seizures , 1995, The Annals of pharmacotherapy.

[128]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[129]  M. Avoli,et al.  Potassium channel activators counteract anoxic hyperexcitability but not 4-aminopyridine-induced epileptiform activity in the rat hippocampal slice , 1994, Neuropharmacology.

[130]  P. E. Sharp,et al.  Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[131]  A. Constanti,et al.  Persistent muscarinic excitation in guinea-pig olfactory cortex neurons: Involvement of a slow post-stimulus afterdepolarizing current , 1993, Neuroscience.

[132]  M. Avoli,et al.  Membrane properties of rat subicular neurons in vitro. , 1993, Journal of neurophysiology.

[133]  A. Colino,et al.  Carbachol Potentiates Q Current and Activates a Calcium‐dependent Non‐specific Conductance in Rat Hippocampus In Vitro , 1993, The European journal of neuroscience.

[134]  J. Lisman,et al.  Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state , 1993, Nature.

[135]  R K Wong,et al.  Intrinsic properties and evoked responses of guinea pig subicular neurons in vitro. , 1993, Journal of neurophysiology.

[136]  A. Alonso,et al.  Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. , 1993, Journal of neurophysiology.

[137]  A. Alonso,et al.  Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. , 1993, Journal of neurophysiology.

[138]  D DiFrancesco,et al.  Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. , 1993, Journal of neurophysiology.

[139]  B H Gähwiler,et al.  Characterization of a Calcium‐dependent Current Generating a Slow Afterdepolarization of CA3 Pyramidal Cells in Rat Hippocampal Slice Cultures , 1993, The European journal of neuroscience.

[140]  A. Mason,et al.  Electrophysiology and burst-firing of rat subicular pyramidal neurons in vitro: a comparison with area CA1 , 1993, Brain Research.

[141]  M. Steriade,et al.  Voltage-dependent fast (20–40 Hz) oscillations in long-axoned neocortical neurons , 1992, Neuroscience.

[142]  R. Llinás,et al.  Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea pig brain in vitro , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[143]  David A. McCormick,et al.  Cellular mechanisms underlying cholinergic and noradrenergic modulation of neuronal firing mode in the cat and guinea pig dorsal lateral geniculate nucleus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[144]  M. Avoli,et al.  4-aminopyridine-induced epileptiform activity and a GABA-mediated long- lasting depolarization in the rat hippocampus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[145]  P. Reiner,et al.  Hyperpolarization-activated inward current in histaminergic tuberomammillary neurons of the rat hypothalamus. , 1991, Journal of neurophysiology.

[146]  C. Y. Yim,et al.  Intrinsic membrane potential oscillations in hippocampal neurons in vitro , 1991, Brain Research.

[147]  Rodrigo Andrade,et al.  Cell excitation enhances muscarinic cholinergic responses in rat association cortex , 1991, Brain Research.

[148]  M. Avoli,et al.  Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. , 1991, Journal of neurophysiology.

[149]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[150]  J. Gaiarsa,et al.  GABA mediated excitation in immature rat CA3 hippocampal neurons , 1990, International Journal of Developmental Neuroscience.

[151]  D. McCormick,et al.  Properties of a hyperpolarization‐activated cation current and its role in rhythmic oscillation in thalamic relay neurones. , 1990, The Journal of physiology.

[152]  M. Witter,et al.  Heterogeneity in the Dorsal Subiculum of the Rat. Distinct Neuronal Zones Project to Different Cortical and Subcortical Targets , 1990, The European journal of neuroscience.

[153]  F. H. Lopes da Silva,et al.  Anatomic organization and physiology of the limbic cortex. , 1990, Physiological reviews.

[154]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[155]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[156]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[157]  R. Llinás,et al.  Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II , 1989, Nature.

[158]  Y. Ben-Ari,et al.  Giant synaptic potentials in immature rat CA3 hippocampal neurones. , 1989, The Journal of physiology.

[159]  D. Davies,et al.  Senile plaques are concentrated in the subicular region of the hippocampal formation in Alzheimer's disease , 1988, Neuroscience Letters.

[160]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

[161]  P. Schwindt,et al.  Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. , 1988, Journal of neurophysiology.

[162]  D. Hinton,et al.  Monoclonal antibody identification of subpopulations of cerebral cortical neurons affected in Alzheimer disease. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[163]  P. Schwindt,et al.  Anomalous rectification in neurons from cat sensorimotor cortex in vitro. , 1987, Journal of neurophysiology.

[164]  R Llinás,et al.  Long-term modifiability of anomalous and delayed rectification in guinea pig inferior olivary neurons , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[165]  B. H. Bland The physiology and pharmacology of hippocampal formation theta rhythms , 1986, Progress in Neurobiology.

[166]  D. Johnston,et al.  Synaptic events underlying spontaneous and evoked paroxysmal discharges in hippocampal neurons. , 1986, Advances in experimental medicine and biology.

[167]  P. Schwartzkroin,et al.  Spontaneous Rhythmic Synchronous Activity in Epileptic Human and Normal Monkey Temporal Lobe , 1986, Epilepsia.

[168]  Z. Bortolotto,et al.  Seizures produced by pilocarpine in mice: A behavioral, electroencephalographic and morphological analysis , 1984, Brain Research.

[169]  P. Schwindt,et al.  Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. , 1984, Journal of neurophysiology.

[170]  E. Cavalheiro,et al.  Limbic seizures produced by pilocarpine in rats: Behavioural, electroencephalographic and neuropathological study , 1983, Behavioural Brain Research.

[171]  C. Wasterlain,et al.  Chemical kindling by muscarinic amygdaloid stimulation in the rat , 1983, Brain Research.

[172]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[173]  B. Connors,et al.  Mechanisms of neocortical epileptogenesis in vitro. , 1982, Journal of neurophysiology.

[174]  Paul R. Adams,et al.  Voltage-clamp analysis of muscarinic excitation in hippocampal neurons , 1982, Brain Research.

[175]  D. Riche,et al.  Long-term effects of intrahippocampal kainic acid injection in rats: a method for inducing spontaneous recurrent seizures. , 1982, Electroencephalography and clinical neurophysiology.

[176]  J. McNamara,et al.  Seizures down-regulate muscarinic cholinergic receptors in hippocampal formation , 1982, Brain Research.

[177]  J. McNamara,et al.  Evidence for an agonist independent down regulation of hippocampal muscarinic receptors in kindling , 1980, Brain Research.

[178]  D. A. Brown,et al.  Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone , 1980, Nature.

[179]  D L Rosene,et al.  Subicular input from temporal cortex in the rhesus monkey. , 1979, Science.

[180]  Y. Ben‐Ari,et al.  A new model of focal status epilepticus: intra-amygdaloid application of kainic acid elicits repetitive secondarily generalized convulsive seizures , 1979, Brain Research.

[181]  J. Nadler,et al.  Kainic acid: neurophysiological and neurotoxic actions. , 1979, Life sciences.

[182]  D. Prince,et al.  Participation of calcium spikes during intrinsic burst firing in hippocampal neurons , 1978, Brain Research.

[183]  Y. Ben-Ari,et al.  [Epileptogenic action of intra-amygdaloid injection of kainic acid]. , 1978, Comptes rendus hebdomadaires des seances de l'Academie des sciences. Serie D: Sciences naturelles.

[184]  D. Prince,et al.  Cellular and field potential properties of epileptogenic hippocampal slices , 1978, Brain Research.

[185]  G F Ayala,et al.  Genesis of epileptic interictal spikes. New knowledge of cortical feedback systems suggests a neurophysiological explanation of brief paroxysms. , 1973, Brain research.

[186]  D. Prince,et al.  Electrophysiology of "epileptic" neurons: spike generation. , 1969, Electroencephalography and clinical neurophysiology.

[187]  C. A. Marsan,et al.  CORTICAL CELLULAR PHENOMENA IN EXPERIMENTAL EPILEPSY: INTERICTAL MANIFESTATIONS. , 1964, Experimental neurology.

[188]  V. Deulofeu [Physiology and pharmacology]. , 1951, Medicina.

[189]  D. B. Tower,et al.  Acetylcholine and neuronal activity; acetylcholine and cholines terase activity in the cerebrospinal fluids of patients with epilepsy. , 1949, Canadian journal of research.

[190]  Trevor Coward,et al.  An In-Vitro Study , 2016 .

[191]  M. Avoli,et al.  Lacosamide , 2009, CNS drugs.

[192]  M. Avoli,et al.  Impaired activation of CA3 pyramidal neurons in the epileptic hippocampus , 2007, NeuroMolecular Medicine.

[193]  J. Taube Electrophysiological properties of neurons in the rat subiculum in vitro , 2004, Experimental Brain Research.

[194]  L Menendez de la Prida,et al.  Electrophysiological and morphological diversity of neurons from the rat subicular complex in vitro , 2003, Hippocampus.

[195]  Giuseppe Biagini,et al.  Limbic network interactions leading to hyperexcitability in a model of temporal lobe epilepsy. , 2002, Journal of neurophysiology.

[196]  M. Avoli,et al.  Electrophysiology of regular firing cells in the rat perirhinal cortex , 2001, Hippocampus.

[197]  F. H. Lopes da Silva,et al.  Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat , 2001, Hippocampus.

[198]  P E Sharp,et al.  Complimentary roles for hippocampal versus subicular/entorhinal place cells in coding place, context, and events , 1999, Hippocampus.

[199]  M. Avoli,et al.  In vitro electrophysiology of rat subicular bursting neurons , 1997, Hippocampus.

[200]  J. Taube Place cells recorded in the parasubiculum of freely moving rats , 1995, Hippocampus.

[201]  I. Soltesz,et al.  The direct perforant path input to CA1: Excitatory or inhibitory? , 1995, Hippocampus.

[202]  K. Krnjević,et al.  Chapter 34: Central cholinergic mechanisms and function , 1993 .

[203]  K. Krnjević,et al.  Central cholinergic mechanisms and function. , 1993, Progress in brain research.

[204]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[205]  Z. Bortolotto,et al.  Review: Cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: A novel experimental model of intractable epilepsy , 1989, Synapse.

[206]  P. Schwindt,et al.  Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. , 1985, Journal of neurophysiology.