Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans

High-frequency field ripples occur in the rodent hippocampal formation and are assumed to depend on interneuron type-specific firing patterns, structuring the activity of pyramidal cells. Ripples with similar characteristics are also present in humans, yet their underlying cellular correlates are still unknown. By in vivo recording interneurons and pyramidal cells in the human hippocampal formation, we find that cell type-specific firing patterns and phase-locking on a millisecond timescale can be distinguished during ripples. In particular, pyramidal cells fired preferentially at the highest amplitude of the ripple, but interneurons began to discharge earlier than pyramidal cells. Furthermore, a large fraction of cells were phase-locked to the ripple cycle, but the preferred phase of discharge of interneurons followed the maximum discharge probability of pyramidal neurons. These relationships between human ripples and unit activity are qualitatively similar to that observed in vivo in the rodents, suggesting that their underlying mechanisms are similar.

[1]  J. R.,et al.  Quantitative analysis , 1892, Nature.

[2]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[3]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[4]  J. Hartigan,et al.  The Dip Test of Unimodality , 1985 .

[5]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[6]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[7]  C. Wilson,et al.  Electrical stimulation of the human epileptic limbic cortex. , 1993, Advances in neurology.

[8]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[9]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[10]  G. Buzsáki,et al.  Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks , 1995, Current Opinion in Neurobiology.

[11]  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.

[12]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[13]  C. Wilson,et al.  Paired pulse suppression and facilitation in human epileptogenic hippocampal formation , 1998, Epilepsy Research.

[14]  R. Traub,et al.  Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro , 1998, Nature.

[15]  Tony A. Fields,et al.  Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. Technical note. , 1999, Journal of neurosurgery.

[16]  H. Batjer,et al.  Current results of the surgical management of aneurysms of the basilar apex. , 1999, Neurosurgery.

[17]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[18]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[19]  A. Lörincz,et al.  Physiological patterns in the hippocampo‐entorhinal cortex system , 2000, Hippocampus.

[20]  Roger D. Traub,et al.  A Model of High-Frequency Ripples in the Hippocampus Based on Synaptic Coupling Plus Axon–Axon Gap Junctions between Pyramidal Neurons , 2000, The Journal of Neuroscience.

[21]  J. Csicsvari,et al.  Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events , 2000, Neuron.

[22]  A. Bragin,et al.  Chronic Epileptogenesis Requires Development of a Network of Pathologically Interconnected Neuron Clusters: A Hypothesis , 2000, Epilepsia.

[23]  G. Buzsáki,et al.  Temporal Interaction between Single Spikes and Complex Spike Bursts in Hippocampal Pyramidal Cells , 2001, Neuron.

[24]  Itzhak Fried,et al.  Interictal high‐frequency oscillations (80–500Hz) in the human epileptic brain: Entorhinal cortex , 2002, Annals of neurology.

[25]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.

[26]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[27]  Charles L. Wilson,et al.  Local Generation of Fast Ripples in Epileptic Brain , 2002, The Journal of Neuroscience.

[28]  D. Ringach,et al.  On the classification of simple and complex cells , 2002, Vision Research.

[29]  G. Buzsáki,et al.  Hippocampal network patterns of activity in the mouse , 2003, Neuroscience.

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

[31]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[32]  P. Somogyi,et al.  Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo , 2004, Nature Neuroscience.

[33]  Charles L. Wilson,et al.  High‐frequency Oscillations after Status Epilepticus: Epileptogenesis and Seizure Genesis , 2004, Epilepsia.

[34]  Charles L. Wilson,et al.  High‐frequency oscillations recorded in human medial temporal lobe during sleep , 2004, Annals of neurology.

[35]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[36]  G. Buzsáki,et al.  Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups , 2005, Neuroscience.

[37]  U. Heinemann,et al.  Induction of sharp wave–ripple complexes in vitro and reorganization of hippocampal networks , 2005, Nature Neuroscience.

[38]  P. Somogyi,et al.  Defined types of cortical interneurone structure space and spike timing in the hippocampus , 2005, The Journal of physiology.

[39]  Lynn Hazan,et al.  Klusters, NeuroScope, NDManager: A free software suite for neurophysiological data processing and visualization , 2006, Journal of Neuroscience Methods.

[40]  Michel Le Van Quyen,et al.  The dark side of high-frequency oscillations in the developing brain , 2006, Trends in Neurosciences.

[41]  Michel Le Van Quyen,et al.  Analysis of dynamic brain oscillations: methodological advances , 2007, Trends in Neurosciences.

[42]  Arne D. Ekstrom,et al.  Brain Oscillations Control Timing of Single-Neuron Activity in Humans , 2007, The Journal of Neuroscience.

[43]  B. McNaughton,et al.  EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. , 2007, Journal of neurophysiology.

[44]  J. Born,et al.  Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. , 2007, Brain : a journal of neurology.

[45]  Guglielmo Foffani,et al.  Reduced Spike-Timing Reliability Correlates with the Emergence of Fast Ripples in the Rat Epileptic Hippocampus , 2007, Neuron.

[46]  Charles L. Wilson,et al.  Characterizing interneuron and pyramidal cells in the human medial temporal lobe in vivo using extracellular recordings , 2007, Hippocampus.

[47]  Jean Gotman,et al.  Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. , 2007, Brain : a journal of neurology.

[48]  P. Dudchenko The hippocampus as a cognitive map , 2010 .