Contralateral dissociation between neural activity and cerebral blood volume during recurrent acute focal neocortical seizures

Sam Harris; Luke W Boorman; Michael Bruyns-Haylett; Aneurin Kennerley; Hongtao Ma; Mingrui Zhao; Paul G Overton; Theodore H Schwartz; Jason Berwick

doi:10.1111/epi.12726

Contralateral dissociation between neural activity and cerebral blood volume during recurrent acute focal neocortical seizures

Sam Harris, Luke W Boorman, Michael Bruyns-Haylett, Aneurin Kennerley, Hongtao Ma, Mingrui Zhao, Paul G Overton, Theodore H Schwartz, Jason Berwick

Chemistry

Research output: Contribution to journal › Article › peer-review

Abstract

OBJECTIVE: Whether epileptic events disrupt normal neurovascular coupling mechanisms locally or remotely is unclear. We sought to investigate neurovascular coupling in an acute model of focal neocortical epilepsy, both within the seizure onset zone and in contralateral homotopic cortex.

METHODS: Neurovascular coupling in both ipsilateral and contralateral vibrissal cortices of the urethane-anesthetized rat were examined during recurrent 4-aminopyridine (4-AP, 15 mm, 1 μl) induced focal seizures. Local field potential (LFP) and multiunit spiking activity (MUA) were recorded via two bilaterally implanted 16-channel microelectrodes. Concurrent two-dimensional optical imaging spectroscopy was used to produce spatiotemporal maps of cerebral blood volume (CBV).

RESULTS: Recurrent acute seizures in right vibrissal cortex (RVC) produced robust ipsilateral increases in LFP and MUA activity, most prominently in layer 5, that were nonlinearly correlated to local increases in CBV. In contrast, contralateral left vibrissal cortex (LVC) exhibited relatively smaller nonlaminar specific increases in neural activity coupled with a decrease in CBV, suggestive of dissociation between neural and hemodynamic responses.

SIGNIFICANCE: These findings provide insights into the impact of epileptic events on the neurovascular unit, and have important implications both for the interpretation of perfusion-based imaging signals in the disorder and understanding the widespread effects of epilepsy. A PowerPoint slide summarizing this article is available for download in the Supporting Information section here.

Original language	English
Pages (from-to)	1423-30
Number of pages	8
Journal	Epilepsia
Volume	55
Issue number	9
DOIs	https://doi.org/10.1111/epi.12726
Publication status	Published - 15 Sept 2014

Keywords

4-Aminopyridine
Animals
Brain Mapping
Cerebrovascular Circulation
Disease Models, Animal
Electroencephalography
Epilepsy
Female
Functional Laterality
Hemodynamics
Potassium Channel Blockers
Rats
Recurrence
Somatosensory Cortex
Statistics, Nonparametric
Journal Article
Research Support, Non-U.S. Gov't

Access to Document

10.1111/epi.12726

Cite this

@article{96e31dc2c280421b8f22fb972909a995,

title = "Contralateral dissociation between neural activity and cerebral blood volume during recurrent acute focal neocortical seizures",

abstract = "OBJECTIVE: Whether epileptic events disrupt normal neurovascular coupling mechanisms locally or remotely is unclear. We sought to investigate neurovascular coupling in an acute model of focal neocortical epilepsy, both within the seizure onset zone and in contralateral homotopic cortex.METHODS: Neurovascular coupling in both ipsilateral and contralateral vibrissal cortices of the urethane-anesthetized rat were examined during recurrent 4-aminopyridine (4-AP, 15 mm, 1 μl) induced focal seizures. Local field potential (LFP) and multiunit spiking activity (MUA) were recorded via two bilaterally implanted 16-channel microelectrodes. Concurrent two-dimensional optical imaging spectroscopy was used to produce spatiotemporal maps of cerebral blood volume (CBV).RESULTS: Recurrent acute seizures in right vibrissal cortex (RVC) produced robust ipsilateral increases in LFP and MUA activity, most prominently in layer 5, that were nonlinearly correlated to local increases in CBV. In contrast, contralateral left vibrissal cortex (LVC) exhibited relatively smaller nonlaminar specific increases in neural activity coupled with a decrease in CBV, suggestive of dissociation between neural and hemodynamic responses.SIGNIFICANCE: These findings provide insights into the impact of epileptic events on the neurovascular unit, and have important implications both for the interpretation of perfusion-based imaging signals in the disorder and understanding the widespread effects of epilepsy. A PowerPoint slide summarizing this article is available for download in the Supporting Information section here.",

keywords = "4-Aminopyridine, Animals, Brain Mapping, Cerebrovascular Circulation, Disease Models, Animal, Electroencephalography, Epilepsy, Female, Functional Laterality, Hemodynamics, Potassium Channel Blockers, Rats, Recurrence, Somatosensory Cortex, Statistics, Nonparametric, Journal Article, Research Support, Non-U.S. Gov't",

author = "Sam Harris and Boorman, {Luke W} and Michael Bruyns-Haylett and Aneurin Kennerley and Hongtao Ma and Mingrui Zhao and Overton, {Paul G} and Schwartz, {Theodore H} and Jason Berwick",

note = "{\textcopyright} 2014 The Authors. Epilepsia published by Wiley Periodicals, Inc. on behalf of International League Against Epilepsy.",

year = "2014",

month = sep,

day = "15",

doi = "10.1111/epi.12726",

language = "English",

volume = "55",

pages = "1423--30",

journal = "Epilepsia",

issn = "0013-9580",

publisher = "Wiley-Blackwell",

number = "9",

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TY - JOUR

T1 - Contralateral dissociation between neural activity and cerebral blood volume during recurrent acute focal neocortical seizures

AU - Harris, Sam

AU - Boorman, Luke W

AU - Bruyns-Haylett, Michael

AU - Kennerley, Aneurin

AU - Ma, Hongtao

AU - Zhao, Mingrui

AU - Overton, Paul G

AU - Schwartz, Theodore H

AU - Berwick, Jason

PY - 2014/9/15

Y1 - 2014/9/15

N2 - OBJECTIVE: Whether epileptic events disrupt normal neurovascular coupling mechanisms locally or remotely is unclear. We sought to investigate neurovascular coupling in an acute model of focal neocortical epilepsy, both within the seizure onset zone and in contralateral homotopic cortex.METHODS: Neurovascular coupling in both ipsilateral and contralateral vibrissal cortices of the urethane-anesthetized rat were examined during recurrent 4-aminopyridine (4-AP, 15 mm, 1 μl) induced focal seizures. Local field potential (LFP) and multiunit spiking activity (MUA) were recorded via two bilaterally implanted 16-channel microelectrodes. Concurrent two-dimensional optical imaging spectroscopy was used to produce spatiotemporal maps of cerebral blood volume (CBV).RESULTS: Recurrent acute seizures in right vibrissal cortex (RVC) produced robust ipsilateral increases in LFP and MUA activity, most prominently in layer 5, that were nonlinearly correlated to local increases in CBV. In contrast, contralateral left vibrissal cortex (LVC) exhibited relatively smaller nonlaminar specific increases in neural activity coupled with a decrease in CBV, suggestive of dissociation between neural and hemodynamic responses.SIGNIFICANCE: These findings provide insights into the impact of epileptic events on the neurovascular unit, and have important implications both for the interpretation of perfusion-based imaging signals in the disorder and understanding the widespread effects of epilepsy. A PowerPoint slide summarizing this article is available for download in the Supporting Information section here.

AB - OBJECTIVE: Whether epileptic events disrupt normal neurovascular coupling mechanisms locally or remotely is unclear. We sought to investigate neurovascular coupling in an acute model of focal neocortical epilepsy, both within the seizure onset zone and in contralateral homotopic cortex.METHODS: Neurovascular coupling in both ipsilateral and contralateral vibrissal cortices of the urethane-anesthetized rat were examined during recurrent 4-aminopyridine (4-AP, 15 mm, 1 μl) induced focal seizures. Local field potential (LFP) and multiunit spiking activity (MUA) were recorded via two bilaterally implanted 16-channel microelectrodes. Concurrent two-dimensional optical imaging spectroscopy was used to produce spatiotemporal maps of cerebral blood volume (CBV).RESULTS: Recurrent acute seizures in right vibrissal cortex (RVC) produced robust ipsilateral increases in LFP and MUA activity, most prominently in layer 5, that were nonlinearly correlated to local increases in CBV. In contrast, contralateral left vibrissal cortex (LVC) exhibited relatively smaller nonlaminar specific increases in neural activity coupled with a decrease in CBV, suggestive of dissociation between neural and hemodynamic responses.SIGNIFICANCE: These findings provide insights into the impact of epileptic events on the neurovascular unit, and have important implications both for the interpretation of perfusion-based imaging signals in the disorder and understanding the widespread effects of epilepsy. A PowerPoint slide summarizing this article is available for download in the Supporting Information section here.

KW - 4-Aminopyridine

KW - Animals

KW - Brain Mapping

KW - Cerebrovascular Circulation

KW - Disease Models, Animal

KW - Electroencephalography

KW - Epilepsy

KW - Female

KW - Functional Laterality

KW - Hemodynamics

KW - Potassium Channel Blockers

KW - Rats

KW - Recurrence

KW - Somatosensory Cortex

KW - Statistics, Nonparametric

KW - Journal Article

KW - Research Support, Non-U.S. Gov't

U2 - 10.1111/epi.12726

DO - 10.1111/epi.12726

M3 - Article

C2 - 25053117

SN - 0013-9580

VL - 55

SP - 1423

EP - 1430

JO - Epilepsia

JF - Epilepsia

IS - 9

ER -