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.

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Acknowledgements

This work was performed at Korea Institute of Science and Technology and was supported in part by U.S. Veterans Administration, US National Institutes of Health Grant RO1 MH039683, the National Research Council of Science and technology of Korea (CRC-15-04-KIST) and the National Research Foundation of Korea (2017R1A2B3012659). REB and JTM received partial salary support from United States VA Biomedical Laboratory Research and Development Service Award I01BX001356. JMM is supported by VA CDA IK2BX002130. Additional salary support was provided by US National Institutes of Health Grants R01 MH100820, R21 NS079866 and R21 NS093000. REB, JTM and JMM are Research Health Scientists at VA Boston Healthcare System. The contents of this work do not represent the views of the U.S. Department of Veterans Affairs or the United States Government. This work also reflects the intellectual contribution and mentorship of Prof. Robert W. McCarley, who sadly passed away during the final stages of this project.

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Correspondence to Jee Hyun Choi.

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The authors report no competing financial interests. JTM also received partial salary compensation and funding from Merck MISP (Merck Investigator Sponsored Programs) but has no conflict of interest with this work.

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Hwang, E., Brown, R.E., Kocsis, B. et al. Optogenetic stimulation of basal forebrain parvalbumin neurons modulates the cortical topography of auditory steady-state responses. Brain Struct Funct 224, 1505–1518 (2019). https://doi.org/10.1007/s00429-019-01845-5

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Keywords

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