Spatiotemporal dynamics of neocortical excitation and inhibition during human sleep

Intracranial recording is an important diagnostic method routinely used in a number of neurological monitoring scenarios. In recent years, advancements in such recordings have been extended to include unit activity of an ensemble of neurons. However, a detailed functional characterization of excitatory and inhibitory cells has not been attempted in human neocortex, particularly during the sleep state. Here, we report that such feature discrimination is possible from high-density recordings in the neocortex by using 2D multielectrode arrays. Successful separation of regular-spiking neurons (or bursting cells) from fast-spiking cells resulted in well-defined clusters that each showed unique intrinsic firing properties. The high density of the array, which allowed recording from a large number of cells (up to 90), helped us to identify apparent monosynaptic connections, confirming the excitatory and inhibitory nature of regular-spiking and fast-spiking cells, thus categorized as putative pyramidal cells and interneurons, respectively. Finally, we investigated the dynamics of correlations within each class. A marked exponential decay with distance was observed in the case of excitatory but not for inhibitory cells. Although the amplitude of that decline depended on the timescale at which the correlations were computed, the spatial constant did not. Furthermore, this spatial constant is compatible with the typical size of human columnar organization. These findings provide a detailed characterization of neuronal activity, functional connectivity at the microcircuit level, and the interplay of excitation and inhibition in the human neocortex.

[1]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[2]  B. Silverman,et al.  Using Kernel Density Estimates to Investigate Multimodality , 1981 .

[3]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[4]  K. Horch,et al.  A silicon-based, three-dimensional neural interface: manufacturing processes for an intracortical electrode array , 1991, IEEE Transactions on Biomedical Engineering.

[5]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[6]  D. Contreras,et al.  Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. , 1997, Journal of neurophysiology.

[7]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[8]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[9]  P. Achermann,et al.  Coherence analysis of the human sleep electroencephalogram , 1998, Neuroscience.

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

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

[12]  D. Contreras,et al.  Spatiotemporal Analysis of Local Field Potentials and Unit Discharges in Cat Cerebral Cortex during Natural Wake and Sleep States , 1999, The Journal of Neuroscience.

[13]  G Buzsáki,et al.  Behavior-Dependent States of the Hippocampal Network Affect Functional Clustering of Neurons , 2001, The Journal of Neuroscience.

[14]  W T Blume,et al.  A randomized, controlled trial of surgery for temporal-lobe epilepsy. , 2001, The New England journal of medicine.

[15]  M. Steriade Neuronal Substrates of Sleep and Epilepsy , 2003 .

[16]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[17]  P. Lennie The Cost of Cortical Computation , 2003, Current Biology.

[18]  G. Buzsáki,et al.  Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons , 2004, Trends in Neurosciences.

[19]  Yoon-Kyu Song,et al.  A microelectrode/microelectronic hybrid device for brain implantable neuroprosthesis applications , 2004, IEEE Transactions on Biomedical Engineering.

[20]  G. Buzsáki,et al.  Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. , 2004, Journal of neurophysiology.

[21]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[22]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[23]  E. Callaway,et al.  Excitatory cortical neurons form fine-scale functional networks , 2005, Nature.

[24]  K. Harris Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[25]  D. McCormick,et al.  Neocortical Network Activity In Vivo Is Generated through a Dynamic Balance of Excitation and Inhibition , 2006, The Journal of Neuroscience.

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

[27]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .

[28]  Alain Destexhe,et al.  Inhibition Determines Membrane Potential Dynamics and Controls Action Potential Generation in Awake and Sleeping Cat Cortex , 2007, The Journal of Neuroscience.

[29]  C. Schroeder,et al.  Microphysiology of Epileptiform Activity in Human Neocortex , 2008, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[30]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[31]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

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

[33]  Allen Waziri,et al.  INITIAL SURGICAL EXPERIENCE WITH A DENSE CORTICAL MICROARRAY IN EPILEPTIC PATIENTS UNDERGOING CRANIOTOMY FOR SUBDURAL ELECTRODE IMPLANTATION , 2009, Neurosurgery.

[34]  Nima Dehghani,et al.  The Human K-Complex Represents an Isolated Cortical Down-State , 2009, Science.

[35]  K. Harris,et al.  Laminar Structure of Spontaneous and Sensory-Evoked Population Activity in Auditory Cortex , 2009, Neuron.

[36]  Itzhak Fried,et al.  Large-Scale Microelectrode Recordings of High-Frequency Gamma Oscillations in Human Cortex during Sleep , 2010, The Journal of Neuroscience.

[37]  Ifije E. Ohiorhenuan,et al.  Sparse coding and high-order correlations in fine-scale cortical networks , 2010, Nature.

[38]  Emery N Brown,et al.  Heterogeneous neuronal firing patterns during interictal epileptiform discharges in the human cortex. , 2010, Brain : a journal of neurology.

[39]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[40]  E. Halgren,et al.  Laminar analysis of slow wave activity in humans. , 2010, Brain : a journal of neurology.

[41]  E. Halgren,et al.  Single-neuron dynamics in human focal epilepsy , 2011, Nature Neuroscience.

[42]  Joseph R. Madsen,et al.  Individualized localization and cortical surface-based registration of intracranial electrodes , 2012, NeuroImage.