Skip to main content
Top
Published in: Brain Structure and Function 4/2019

01-05-2019 | Original Article

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

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

Published in: Brain Structure and Function | Issue 4/2019

Login to get access

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.
Appendix
Available only for authorised users
Literature
go back to reference Berger H (1929) Ueber das elektroenkephalogramm des Menschen. Arch Psychiatr Nervenkr 87:527–570CrossRef Berger H (1929) Ueber das elektroenkephalogramm des Menschen. Arch Psychiatr Nervenkr 87:527–570CrossRef
go back to reference Burk JA, Sarter M (2001) Dissociation between the attentional functions mediated via basal forebrain cholinergic and GABAergic neurons. Neuroscience 105(4):899–909CrossRefPubMed Burk JA, Sarter M (2001) Dissociation between the attentional functions mediated via basal forebrain cholinergic and GABAergic neurons. Neuroscience 105(4):899–909CrossRefPubMed
go back to reference Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459(7247):663–667CrossRefPubMedPubMedCentral Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459(7247):663–667CrossRefPubMedPubMedCentral
go back to reference Carlen M, Meletis K, Siegle JH, Cardin JA, Futai K, Vierling-Claassen D, Ruhlmann C, Jones SR, Deisseroth K, Sheng M, Moore CI, Tsai LH (2012) A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry 17:537–548CrossRefPubMed Carlen M, Meletis K, Siegle JH, Cardin JA, Futai K, Vierling-Claassen D, Ruhlmann C, Jones SR, Deisseroth K, Sheng M, Moore CI, Tsai LH (2012) A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry 17:537–548CrossRefPubMed
go back to reference Choi JH, Koch KP, Poppendieck W, Lee M, Shin HS (2010) High resolution electroencephalography in freely moving mice. J Neurophysiol 104(3):1825–1834CrossRefPubMed Choi JH, Koch KP, Poppendieck W, Lee M, Shin HS (2010) High resolution electroencephalography in freely moving mice. J Neurophysiol 104(3):1825–1834CrossRefPubMed
go back to reference Crone NE, Boatman D, Gordon B, Hao L (2001) Induced electrocorticographic gamma activity during auditory perception. Brazier Award-winning article, 2001. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 112(4):565–582CrossRef Crone NE, Boatman D, Gordon B, Hao L (2001) Induced electrocorticographic gamma activity during auditory perception. Brazier Award-winning article, 2001. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 112(4):565–582CrossRef
go back to reference Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70(2):200–227CrossRefPubMed Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70(2):200–227CrossRefPubMed
go back to reference Duque A, Balatoni B, Detari L, Zaborszky L (2000) EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 84(3):1627–1635CrossRefPubMed Duque A, Balatoni B, Detari L, Zaborszky L (2000) EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 84(3):1627–1635CrossRefPubMed
go back to reference Franklin K, Paxinos G (2008) The mouse brain in stereotaxic coordinates, 3rd edn. Academic Press, North Ryde Franklin K, Paxinos G (2008) The mouse brain in stereotaxic coordinates, 3rd edn. Academic Press, North Ryde
go back to reference Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224CrossRefPubMed Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224CrossRefPubMed
go back to reference Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86(5):1698–1702CrossRefPubMed Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86(5):1698–1702CrossRefPubMed
go back to reference Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324(5931):1207–1210CrossRefPubMedPubMedCentral Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324(5931):1207–1210CrossRefPubMedPubMedCentral
go back to reference Kim T, Thankachan S, McKenna JT, McNally JM, Yang C, Choi JH, Chen L, Kocsis B, Deisseroth K, Strecker RE, Basheer R, Brown RE, McCarley RW (2015) Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc Natl Acad Sci USA 112(11):3535–3540CrossRefPubMed Kim T, Thankachan S, McKenna JT, McNally JM, Yang C, Choi JH, Chen L, Kocsis B, Deisseroth K, Strecker RE, Basheer R, Brown RE, McCarley RW (2015) Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc Natl Acad Sci USA 112(11):3535–3540CrossRefPubMed
go back to reference Korotkova T, Fuchs EC, Ponomarenko A, von EJ, Monyer H (2010) NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68(3):557–569CrossRefPubMed Korotkova T, Fuchs EC, Ponomarenko A, von EJ, Monyer H (2010) NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68(3):557–569CrossRefPubMed
go back to reference Kwon JS, O’Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton ME, McCarley RW (1999) Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry 56(11):1001–1005CrossRefPubMedPubMedCentral Kwon JS, O’Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton ME, McCarley RW (1999) Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry 56(11):1001–1005CrossRefPubMedPubMedCentral
go back to reference Linden RD, Campbell KB, Hamel G, Picton TW (1985) Human auditory steady state evoked potentials during sleep. Ear Hear 6(3):167–174CrossRefPubMed Linden RD, Campbell KB, Hamel G, Picton TW (1985) Human auditory steady state evoked potentials during sleep. Ear Hear 6(3):167–174CrossRefPubMed
go back to reference McKenna JT, Yang C, Franciosi S, Winston S, Abarr KK, Rigby MS, Yanagawa Y, McCarley RW, Brown RE (2013) Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. J Comp Neurol 521:1225–1250CrossRefPubMedPubMedCentral McKenna JT, Yang C, Franciosi S, Winston S, Abarr KK, Rigby MS, Yanagawa Y, McCarley RW, Brown RE (2013) Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. J Comp Neurol 521:1225–1250CrossRefPubMedPubMedCentral
go back to reference Munk MH, Roelfsema PR, Konig P, Engel AK, Singer W (1996) Role of reticular activation in the modulation of intracortical synchronization. Science 272(5259):271–274CrossRefPubMed Munk MH, Roelfsema PR, Konig P, Engel AK, Singer W (1996) Role of reticular activation in the modulation of intracortical synchronization. Science 272(5259):271–274CrossRefPubMed
go back to reference O’Donnell BF, Vohs JL, Krishnan GP, Rass O, Hetrick WP, Morzorati SL (2013) The auditory steady-state response (ASSR): a translational biomarker for schizophrenia. Suppl Clin Neurophysiol 62:101–112CrossRefPubMedPubMedCentral O’Donnell BF, Vohs JL, Krishnan GP, Rass O, Hetrick WP, Morzorati SL (2013) The auditory steady-state response (ASSR): a translational biomarker for schizophrenia. Suppl Clin Neurophysiol 62:101–112CrossRefPubMedPubMedCentral
go back to reference Plourde G (1996) The effects of propofol on the 40-Hz auditory steady-state response and on the electroencephalogram in humans. Anesth Analg 82(5):1015–1022PubMed Plourde G (1996) The effects of propofol on the 40-Hz auditory steady-state response and on the electroencephalogram in humans. Anesth Analg 82(5):1015–1022PubMed
go back to reference Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini M (2009) Natural frequencies of human corticothalamic circuits. J Neurosci 29(24):7679–7685CrossRefPubMedPubMedCentral Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini M (2009) Natural frequencies of human corticothalamic circuits. J Neurosci 29(24):7679–7685CrossRefPubMedPubMedCentral
go back to reference Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459(7247):698–702CrossRefPubMedPubMedCentral Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459(7247):698–702CrossRefPubMedPubMedCentral
go back to reference Spencer KM, Salisbury DF, Shenton ME, McCarley RW (2008) Gamma-band auditory steady-state responses are impaired in first episode psychosis. Biol Psychiatry 64(5):369–375CrossRefPubMedPubMedCentral Spencer KM, Salisbury DF, Shenton ME, McCarley RW (2008) Gamma-band auditory steady-state responses are impaired in first episode psychosis. Biol Psychiatry 64(5):369–375CrossRefPubMedPubMedCentral
go back to reference Spencer KM, Niznikiewicz MA, Nestor PG, Shenton ME, McCarley RW (2009) Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC Neurosci 10:85CrossRefPubMedPubMedCentral Spencer KM, Niznikiewicz MA, Nestor PG, Shenton ME, McCarley RW (2009) Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC Neurosci 10:85CrossRefPubMedPubMedCentral
go back to reference Tiitinen H, Sinkkonen J, Reinikainen K, Alho K, Lavikainen J, Naatanen R (1993) Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364(6432):59–60CrossRefPubMed Tiitinen H, Sinkkonen J, Reinikainen K, Alho K, Lavikainen J, Naatanen R (1993) Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364(6432):59–60CrossRefPubMed
Metadata
Title
Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses
Authors
Eunjin Hwang
Ritchie E. Brown
Bernat Kocsis
Tae Kim
James T. McKenna
James M. McNally
Hio-Been Han
Jee Hyun Choi
Publication date
01-05-2019
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 4/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-019-01845-5

Other articles of this Issue 4/2019

Brain Structure and Function 4/2019 Go to the issue