Impact of cognitive stimulation on ripples within human epileptic and non-epileptic hippocampus

BackgroundUntil now there has been no way of distinguishing between physiological and epileptic hippocampal ripples in intracranial recordings. In the present study we addressed this by investigating the effect of cognitive stimulation on interictal high frequency oscillations in the ripple range (80–250 Hz) within epileptic (EH) and non-epileptic hippocampus (NH).MethodsWe analyzed depth EEG recordings in 10 patients with intractable epilepsy, in whom hippocampal activity was recorded initially during quiet wakefulness and subsequently during a simple cognitive task. Using automated detection of ripples based on amplitude of the power envelope, we analyzed ripple rate (RR) in the cognitive and resting period, within EH and NH.ResultsCompared to quiet wakefulness we observed a significant reduction of RR during cognitive stimulation in EH, while it remained statistically marginal in NH. Further, we investigated the direct impact of cognitive stimuli on ripples (i.e. immediately post-stimulus), which showed a transient statistically significant suppression of ripples in the first second after stimuli onset in NH only.ConclusionOur results point to a differential reactivity of ripples within EH and NH to cognitive stimulation.

[1]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

[2]  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.

[3]  Charles L. Wilson,et al.  Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans , 2008, The Journal of Neuroscience.

[4]  Michal Mikl,et al.  Combined event-related fMRI and intracerebral ERP study of an auditory oddball task , 2005, NeuroImage.

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

[6]  C. Dickson,et al.  Short-duration epileptic discharges show a distinct phase preference during ongoing hippocampal slow oscillations. , 2010, Journal of neurophysiology.

[7]  A. Davies,et al.  Intrinsic programmes of growth and survival in developing vertebrate neurons , 1994, Trends in Neurosciences.

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

[9]  Margaret F. Carr,et al.  Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval , 2011, Nature Neuroscience.

[10]  Mark R. Bower,et al.  High frequency oscillations are associated with cognitive processing in human recognition memory. , 2014, Brain : a journal of neurology.

[11]  Matthew A. Wilson,et al.  Hippocampal Replay of Extended Experience , 2009, Neuron.

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

[13]  J. Talairach Atlas d'anatomie stéréotaxique du télencéphale : études anatomo-radiologiques , 1967 .

[14]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[15]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[16]  Edgar M. Housepian Atlas d'anatomie stereotaxique du telencephale. , 1968 .

[17]  Markku Penttonen,et al.  This Reprint May Differ from the Original in Pagination and Typographic Detail. Disrupting Neural Activity Related to Awake-state Sharp Wave-ripple Complexes Prevents Hippocampal Learning Disrupting Neural Activity Related to Awake-state Sharp Wave-ripple Complexes Prevents Hippocampal Learning , 2022 .

[18]  J. Fell,et al.  Ripples in the medial temporal lobe are relevant for human memory consolidation. , 2008, Brain : a journal of neurology.

[19]  Matthijs A. A. van der Meer,et al.  Hippocampal Replay Is Not a Simple Function of Experience , 2010, Neuron.

[20]  J. Martinerie,et al.  Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. , 2010, Brain : a journal of neurology.

[21]  Fernando Lopes da Silva,et al.  High-frequency oscillations – Where we are and where we need to go , 2012, Progress in Neurobiology.

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

[23]  J. Gotman,et al.  High-frequency oscillations (HFOs) in clinical epilepsy , 2012, Progress in Neurobiology.

[24]  Attila I. Gulyás,et al.  Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation , 2015, Current Opinion in Neurobiology.

[25]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[26]  Michaël Zugaro,et al.  Hippocampal ripples and memory consolidation , 2011, Current Opinion in Neurobiology.

[27]  G. Buzsáki Hippocampal sharp waves: Their origin and significance , 1986, Brain Research.

[28]  E. Fetz,et al.  Decoupling the Cortical Power Spectrum Reveals Real-Time Representation of Individual Finger Movements in Humans , 2009, The Journal of Neuroscience.

[29]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  J. O’Neill,et al.  Place-Selective Firing of CA1 Pyramidal Cells during Sharp Wave/Ripple Network Patterns in Exploratory Behavior , 2006, Neuron.

[31]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[32]  J. Gotman,et al.  Effect of sleep stage on interictal high‐frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy , 2009, Epilepsia.

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

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

[35]  György Buzsáki,et al.  High frequency oscillations in the intact brain , 2012, Progress in Neurobiology.

[36]  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.

[37]  B. Brinkmann,et al.  Pathological and physiological high-frequency oscillations in focal human epilepsy. , 2013, Journal of neurophysiology.

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

[39]  D. Dinner,et al.  Effect of Sleep on Epilepsy , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[41]  I. Módy,et al.  High-frequency oscillations : What is normal and what is not ? , 2008 .

[42]  B. McNaughton,et al.  Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics , 1999, The Journal of Neuroscience.

[43]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[44]  R. Kempter,et al.  Coherent Phasic Excitation during Hippocampal Ripples , 2011, Neuron.

[45]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.