Microscale spatiotemporal dynamics during neocortical propagation of human focal seizures.
NeuroImage. 2015-11-01; 122: 114-130
DOI: 10.1016/j.neuroimage.2015.08.019
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1. Neuroimage. 2015 Nov 15;122:114-30. doi: 10.1016/j.neuroimage.2015.08.019. Epub
2015 Aug 14.
Microscale spatiotemporal dynamics during neocortical propagation of human focal
seizures.
Wagner FB(1), Eskandar EN(2), Cosgrove GR(3), Madsen JR(4), Blum AS(5), Potter
NS(5), Hochberg LR(6), Cash SS(7), Truccolo W(8).
Author information:
(1)Department of Neuroscience, Brown University, Providence, RI, 02912, United
States. Electronic address: .
(2)Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical
School, Boston, MA, 02114, United States; Nayef Al-Rodhan Laboratories for
Cellular Neurosurgery and Neurosurgical Technology, Massachusetts General
Hospital and Harvard Medical School, Boston, MA, 02114, United States.
(3)Department of Neurosurgery, Alpert Medical School, Brown University,
Providence, RI, 02912, United States; Norman Prince Neurosciences Institute,
Brown University, Providence, RI, 02912, United States.
(4)Department of Neurosurgery, Children’s Hospital and Harvard Medical School,
Boston, MA, 02114, United States; Department of Neurosurgery, Brigham and Women’s
Hospital and Harvard Medical School, Boston, MA, 02114, United States.
(5)Department of Neurology, Alpert Medical School, Brown University, Providence,
RI, 02912, United States.
(6)School of Engineering, Brown University, Providence, RI, 02912, United States;
Institute for Brain Science, Brown University, Providence, RI, 02912, United
States; Center for Neurorestoration and Neurotechnology, U.S. Department of
Veterans Affairs, Providence, RI, United States; Department of Neurology,
Massachusetts General Hospital and Harvard Medical School, Boston, MA, 02114,
United States; Department of Neurology, Brigham and Women’s Hospital and Harvard
Medical School, Boston, MA, 02114, United States.
(7)Department of Neurology, Massachusetts General Hospital and Harvard Medical
School, Boston, MA, 02114, United States.
(8)Department of Neuroscience, Brown University, Providence, RI, 02912, United
States; Institute for Brain Science, Brown University, Providence, RI, 02912,
United States; Center for Neurorestoration and Neurotechnology, U.S. Department
of Veterans Affairs, Providence, RI, United States. Electronic address:
.
Some of the most clinically consequential aspects of focal epilepsy, e.g. loss of
consciousness, arise from the generalization or propagation of seizures through
local and large-scale neocortical networks. Yet, the dynamics of such neocortical
propagation remain poorly understood. Here, we studied the microdynamics of focal
seizure propagation in neocortical patches (4×4 mm) recorded via high-density
microelectrode arrays (MEAs) implanted in people with pharmacologically resistant
epilepsy. Our main findings are threefold: (1) a newly developed stage
segmentation method, applied to local field potentials (LFPs) and multiunit
activity (MUA), revealed a succession of discrete seizure stages, each lasting
several seconds. These different stages showed characteristic evolutions in
overall activity and spatial patterns, which were relatively consistent across
seizures within each of the 5 patients studied. Interestingly, segmented seizure
stages based on LFPs or MUA showed a dissociation of their spatiotemporal
dynamics, likely reflecting different contributions of non-local synaptic inputs
and local network activity. (2) As previously reported, some of the seizures
showed a peak in MUA that happened several seconds after local seizure onset and
slowly propagated across the MEA. However, other seizures had a more complex
structure characterized by, for example, several MUA peaks, more consistent with
the succession of discrete stages than the slow propagation of a simple wavefront
of increased MUA. In both cases, nevertheless, seizures characterized by
spike-wave discharges (SWDs, ~2-3 Hz) eventually evolved into patterns of
phase-locked MUA and LFPs. (3) Individual SWDs or gamma oscillation cycles (25-60
Hz), characteristic of two different types of recorded seizures, tended to
propagate with varying degrees of directionality, directions of propagation and
speeds, depending on the identified seizure stage. However, no clear relationship
was observed between the MUA peak onset time (in seizures where such peak onset
occurred) and changes in MUA or LFP propagation patterns. Overall, our findings
indicate that the recruitment of neocortical territories into ictal activity
undergoes complex spatiotemporal dynamics evolving in slow discrete states, which
are consistent across seizures within each patient. Furthermore, ictal states at
finer spatiotemporal scales (individual SWDs or gamma oscillations) are organized
by slower time scale network dynamics evolving through these discrete stages.
Copyright © 2015 Elsevier Inc. All rights reserved.
DOI: 10.1016/j.neuroimage.2015.08.019
PMCID: PMC4618174
PMID: 26279211 [Indexed for MEDLINE]