Neuro-oscillatory phase alignment drives speeded multisensory response times

An electro-corticographic investigation

Manuel R. Mercier, Sophie Molholm, Ian C. Fiebelkorn, John S. Butler, Theodore H. Schwartz, John J. Foxe

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

Even simple tasks rely on information exchange between functionally distinct and often relatively distant neuronal ensembles. Considerable work indicates oscillatory synchronization through phase alignment is a major agent of inter-regional communication. In the brain, different oscillatory phases correspond to low-and high-excitability states. Optimally aligned phases (or high-excitability states) promote inter-regional communication. Studies have also shown that sensory stimulation can modulate or reset the phase of ongoing cortical oscillations. For example, auditory stimuli can reset the phase of oscillations in visual cortex, influencing processing of a simultaneous visual stimulus. Such cross-regional phase reset represents a candidate mechanism for aligning oscillatory phase for inter-regional communication. Here, we explored the role of local and inter-regional phase alignment in driving a well established behavioral correlate of multisensory integration: the redundant target effect (RTE), which refers to the fact that responses to multisensory inputs are substantially faster than to unisensory stimuli. In a speeded detection task, human epileptic patients (N _ 3) responded to unisensory (auditory or visual) and multisensory (audiovisual) stimuli with a button press, while electrocorticography was recorded over auditory and motor regions. Visual stimulation significantly modulated auditory activity via phase reset in the delta and theta bands. During the period between stimulation and subsequent motor response, transient synchronization between auditory and motor regions was observed. Phase synchrony to multisensory inputs was faster than to unisensory stimulation. This sensorimotor phase alignment correlated with behavior such that stronger synchrony was associated with faster responses, linking the commonly observed RTE with phase alignment across a sensorimotor network.

Original languageEnglish (US)
Pages (from-to)8546-8557
Number of pages12
JournalJournal of Neuroscience
Volume35
Issue number22
DOIs
StatePublished - Jun 3 2015

Fingerprint

Reaction Time
Communication
Photic Stimulation
Visual Cortex
Brain
Drive
Electrocorticography

Keywords

  • ECoG
  • EEG
  • Motor
  • Multisensory
  • Oscillations
  • Synchrony

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Neuro-oscillatory phase alignment drives speeded multisensory response times : An electro-corticographic investigation. / Mercier, Manuel R.; Molholm, Sophie; Fiebelkorn, Ian C.; Butler, John S.; Schwartz, Theodore H.; Foxe, John J.

In: Journal of Neuroscience, Vol. 35, No. 22, 03.06.2015, p. 8546-8557.

Research output: Contribution to journalArticle

Mercier, Manuel R. ; Molholm, Sophie ; Fiebelkorn, Ian C. ; Butler, John S. ; Schwartz, Theodore H. ; Foxe, John J. / Neuro-oscillatory phase alignment drives speeded multisensory response times : An electro-corticographic investigation. In: Journal of Neuroscience. 2015 ; Vol. 35, No. 22. pp. 8546-8557.
@article{61508ae0a43445ae997cb014440aac51,
title = "Neuro-oscillatory phase alignment drives speeded multisensory response times: An electro-corticographic investigation",
abstract = "Even simple tasks rely on information exchange between functionally distinct and often relatively distant neuronal ensembles. Considerable work indicates oscillatory synchronization through phase alignment is a major agent of inter-regional communication. In the brain, different oscillatory phases correspond to low-and high-excitability states. Optimally aligned phases (or high-excitability states) promote inter-regional communication. Studies have also shown that sensory stimulation can modulate or reset the phase of ongoing cortical oscillations. For example, auditory stimuli can reset the phase of oscillations in visual cortex, influencing processing of a simultaneous visual stimulus. Such cross-regional phase reset represents a candidate mechanism for aligning oscillatory phase for inter-regional communication. Here, we explored the role of local and inter-regional phase alignment in driving a well established behavioral correlate of multisensory integration: the redundant target effect (RTE), which refers to the fact that responses to multisensory inputs are substantially faster than to unisensory stimuli. In a speeded detection task, human epileptic patients (N _ 3) responded to unisensory (auditory or visual) and multisensory (audiovisual) stimuli with a button press, while electrocorticography was recorded over auditory and motor regions. Visual stimulation significantly modulated auditory activity via phase reset in the delta and theta bands. During the period between stimulation and subsequent motor response, transient synchronization between auditory and motor regions was observed. Phase synchrony to multisensory inputs was faster than to unisensory stimulation. This sensorimotor phase alignment correlated with behavior such that stronger synchrony was associated with faster responses, linking the commonly observed RTE with phase alignment across a sensorimotor network.",
keywords = "ECoG, EEG, Motor, Multisensory, Oscillations, Synchrony",
author = "Mercier, {Manuel R.} and Sophie Molholm and Fiebelkorn, {Ian C.} and Butler, {John S.} and Schwartz, {Theodore H.} and Foxe, {John J.}",
year = "2015",
month = "6",
day = "3",
doi = "10.1523/JNEUROSCI.4527-14.2015",
language = "English (US)",
volume = "35",
pages = "8546--8557",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "22",

}

TY - JOUR

T1 - Neuro-oscillatory phase alignment drives speeded multisensory response times

T2 - An electro-corticographic investigation

AU - Mercier, Manuel R.

AU - Molholm, Sophie

AU - Fiebelkorn, Ian C.

AU - Butler, John S.

AU - Schwartz, Theodore H.

AU - Foxe, John J.

PY - 2015/6/3

Y1 - 2015/6/3

N2 - Even simple tasks rely on information exchange between functionally distinct and often relatively distant neuronal ensembles. Considerable work indicates oscillatory synchronization through phase alignment is a major agent of inter-regional communication. In the brain, different oscillatory phases correspond to low-and high-excitability states. Optimally aligned phases (or high-excitability states) promote inter-regional communication. Studies have also shown that sensory stimulation can modulate or reset the phase of ongoing cortical oscillations. For example, auditory stimuli can reset the phase of oscillations in visual cortex, influencing processing of a simultaneous visual stimulus. Such cross-regional phase reset represents a candidate mechanism for aligning oscillatory phase for inter-regional communication. Here, we explored the role of local and inter-regional phase alignment in driving a well established behavioral correlate of multisensory integration: the redundant target effect (RTE), which refers to the fact that responses to multisensory inputs are substantially faster than to unisensory stimuli. In a speeded detection task, human epileptic patients (N _ 3) responded to unisensory (auditory or visual) and multisensory (audiovisual) stimuli with a button press, while electrocorticography was recorded over auditory and motor regions. Visual stimulation significantly modulated auditory activity via phase reset in the delta and theta bands. During the period between stimulation and subsequent motor response, transient synchronization between auditory and motor regions was observed. Phase synchrony to multisensory inputs was faster than to unisensory stimulation. This sensorimotor phase alignment correlated with behavior such that stronger synchrony was associated with faster responses, linking the commonly observed RTE with phase alignment across a sensorimotor network.

AB - Even simple tasks rely on information exchange between functionally distinct and often relatively distant neuronal ensembles. Considerable work indicates oscillatory synchronization through phase alignment is a major agent of inter-regional communication. In the brain, different oscillatory phases correspond to low-and high-excitability states. Optimally aligned phases (or high-excitability states) promote inter-regional communication. Studies have also shown that sensory stimulation can modulate or reset the phase of ongoing cortical oscillations. For example, auditory stimuli can reset the phase of oscillations in visual cortex, influencing processing of a simultaneous visual stimulus. Such cross-regional phase reset represents a candidate mechanism for aligning oscillatory phase for inter-regional communication. Here, we explored the role of local and inter-regional phase alignment in driving a well established behavioral correlate of multisensory integration: the redundant target effect (RTE), which refers to the fact that responses to multisensory inputs are substantially faster than to unisensory stimuli. In a speeded detection task, human epileptic patients (N _ 3) responded to unisensory (auditory or visual) and multisensory (audiovisual) stimuli with a button press, while electrocorticography was recorded over auditory and motor regions. Visual stimulation significantly modulated auditory activity via phase reset in the delta and theta bands. During the period between stimulation and subsequent motor response, transient synchronization between auditory and motor regions was observed. Phase synchrony to multisensory inputs was faster than to unisensory stimulation. This sensorimotor phase alignment correlated with behavior such that stronger synchrony was associated with faster responses, linking the commonly observed RTE with phase alignment across a sensorimotor network.

KW - ECoG

KW - EEG

KW - Motor

KW - Multisensory

KW - Oscillations

KW - Synchrony

UR - http://www.scopus.com/inward/record.url?scp=84930421526&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84930421526&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.4527-14.2015

DO - 10.1523/JNEUROSCI.4527-14.2015

M3 - Article

VL - 35

SP - 8546

EP - 8557

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 22

ER -