Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses

Eunjin Hwang; Ritchie E. Brown; Bernat Kocsis; Tae Kim; James T. McKenna; James M. McNally; Hio Been Han; Jee Hyun Choi

doi:10.1007/s00429-019-01845-5

Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses

Eunjin Hwang
, Ritchie E. Brown
, Bernat Kocsis
, Tae Kim
, James T. McKenna
, James M. McNally
, Hio Been Han
, Jee Hyun Choi

School of Convergence

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

27 Scopus citations

Abstract

High-density electroencephalographic (hdEEG) recordings are widely used in human studies to determine spatio-temporal patterns of cortical electrical activity. How these patterns of activity are modulated by subcortical arousal systems is poorly understood. Here, we couple selective optogenetic stimulation of a defined subcortical cell-type, basal forebrain (BF) parvalbumin (PV) neurons, with hdEEG recordings in mice (Opto-hdEEG). Stimulation of BF PV projection neurons preferentially generated time-locked gamma oscillations in frontal cortices. BF PV gamma-frequency stimulation potently modulated an auditory sensory paradigm used to probe cortical function in neuropsychiatric disorders, the auditory steady-state response (ASSR). Phase-locked excitation of BF PV neurons in advance of 40 Hz auditory stimuli enhanced the power, precision and reliability of cortical responses, and the relationship between responses in frontal and auditory cortices. Furthermore, synchronization within a frontal hub and long-range cortical interactions were enhanced. Thus, phasic discharge of BF PV neurons changes cortical processing in a manner reminiscent of global workspace models of attention and consciousness.

Original language	English
Pages (from-to)	1505-1518
Number of pages	14
Journal	Brain Structure and Function
Volume	224
Issue number	4
DOIs	https://doi.org/10.1007/s00429-019-01845-5
State	Published - 1 May 2019

Keywords

Auditory steady-state response (ASSR)
Basal forebrain
Gamma oscillations
Optogenetic high-density EEG
Parvalbumin

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10.1007/s00429-019-01845-5

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title = "Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses",

abstract = "High-density electroencephalographic (hdEEG) recordings are widely used in human studies to determine spatio-temporal patterns of cortical electrical activity. How these patterns of activity are modulated by subcortical arousal systems is poorly understood. Here, we couple selective optogenetic stimulation of a defined subcortical cell-type, basal forebrain (BF) parvalbumin (PV) neurons, with hdEEG recordings in mice (Opto-hdEEG). Stimulation of BF PV projection neurons preferentially generated time-locked gamma oscillations in frontal cortices. BF PV gamma-frequency stimulation potently modulated an auditory sensory paradigm used to probe cortical function in neuropsychiatric disorders, the auditory steady-state response (ASSR). Phase-locked excitation of BF PV neurons in advance of 40 Hz auditory stimuli enhanced the power, precision and reliability of cortical responses, and the relationship between responses in frontal and auditory cortices. Furthermore, synchronization within a frontal hub and long-range cortical interactions were enhanced. Thus, phasic discharge of BF PV neurons changes cortical processing in a manner reminiscent of global workspace models of attention and consciousness.",

keywords = "Auditory steady-state response (ASSR), Basal forebrain, Gamma oscillations, Optogenetic high-density EEG, Parvalbumin",

author = "Eunjin Hwang and Brown, \{Ritchie E.\} and Bernat Kocsis and Tae Kim and McKenna, \{James T.\} and McNally, \{James M.\} and Han, \{Hio Been\} and Choi, \{Jee Hyun\}",

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doi = "10.1007/s00429-019-01845-5",

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T1 - Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses

AU - Hwang, Eunjin

AU - Brown, Ritchie E.

AU - Kocsis, Bernat

AU - Kim, Tae

AU - McKenna, James T.

AU - McNally, James M.

AU - Han, Hio Been

AU - Choi, Jee Hyun

N1 - Publisher Copyright: © 2019, This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection.

PY - 2019/5/1

Y1 - 2019/5/1

N2 - High-density electroencephalographic (hdEEG) recordings are widely used in human studies to determine spatio-temporal patterns of cortical electrical activity. How these patterns of activity are modulated by subcortical arousal systems is poorly understood. Here, we couple selective optogenetic stimulation of a defined subcortical cell-type, basal forebrain (BF) parvalbumin (PV) neurons, with hdEEG recordings in mice (Opto-hdEEG). Stimulation of BF PV projection neurons preferentially generated time-locked gamma oscillations in frontal cortices. BF PV gamma-frequency stimulation potently modulated an auditory sensory paradigm used to probe cortical function in neuropsychiatric disorders, the auditory steady-state response (ASSR). Phase-locked excitation of BF PV neurons in advance of 40 Hz auditory stimuli enhanced the power, precision and reliability of cortical responses, and the relationship between responses in frontal and auditory cortices. Furthermore, synchronization within a frontal hub and long-range cortical interactions were enhanced. Thus, phasic discharge of BF PV neurons changes cortical processing in a manner reminiscent of global workspace models of attention and consciousness.

AB - High-density electroencephalographic (hdEEG) recordings are widely used in human studies to determine spatio-temporal patterns of cortical electrical activity. How these patterns of activity are modulated by subcortical arousal systems is poorly understood. Here, we couple selective optogenetic stimulation of a defined subcortical cell-type, basal forebrain (BF) parvalbumin (PV) neurons, with hdEEG recordings in mice (Opto-hdEEG). Stimulation of BF PV projection neurons preferentially generated time-locked gamma oscillations in frontal cortices. BF PV gamma-frequency stimulation potently modulated an auditory sensory paradigm used to probe cortical function in neuropsychiatric disorders, the auditory steady-state response (ASSR). Phase-locked excitation of BF PV neurons in advance of 40 Hz auditory stimuli enhanced the power, precision and reliability of cortical responses, and the relationship between responses in frontal and auditory cortices. Furthermore, synchronization within a frontal hub and long-range cortical interactions were enhanced. Thus, phasic discharge of BF PV neurons changes cortical processing in a manner reminiscent of global workspace models of attention and consciousness.

KW - Auditory steady-state response (ASSR)

KW - Basal forebrain

KW - Gamma oscillations

KW - Optogenetic high-density EEG

KW - Parvalbumin

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DO - 10.1007/s00429-019-01845-5

M3 - Article

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JO - Brain Structure and Function

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ER -

Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses

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Keywords

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