Skip to main content
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian
  • Log in
  • My Cart

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses

New Research In

Physical Sciences

Featured Portals

  • Physics
  • Chemistry
  • Sustainability Science

Articles by Topic

  • Applied Mathematics
  • Applied Physical Sciences
  • Astronomy
  • Computer Sciences
  • Earth, Atmospheric, and Planetary Sciences
  • Engineering
  • Environmental Sciences
  • Mathematics
  • Statistics

Social Sciences

Featured Portals

  • Anthropology
  • Sustainability Science

Articles by Topic

  • Economic Sciences
  • Environmental Sciences
  • Political Sciences
  • Psychological and Cognitive Sciences
  • Social Sciences

Biological Sciences

Featured Portals

  • Sustainability Science

Articles by Topic

  • Agricultural Sciences
  • Anthropology
  • Applied Biological Sciences
  • Biochemistry
  • Biophysics and Computational Biology
  • Cell Biology
  • Developmental Biology
  • Ecology
  • Environmental Sciences
  • Evolution
  • Genetics
  • Immunology and Inflammation
  • Medical Sciences
  • Microbiology
  • Neuroscience
  • Pharmacology
  • Physiology
  • Plant Biology
  • Population Biology
  • Psychological and Cognitive Sciences
  • Sustainability Science
  • Systems Biology
Research Article

Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations

Tae Kim, Stephen Thankachan, James T. McKenna, James M. McNally, Chun Yang, Jee Hyun Choi, Lichao Chen, Bernat Kocsis, Karl Deisseroth, Robert E. Strecker, Radhika Basheer, View ORCID ProfileRitchie E. Brown, and Robert W. McCarley
PNAS March 17, 2015 112 (11) 3535-3540; first published March 2, 2015; https://doi.org/10.1073/pnas.1413625112
Tae Kim
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stephen Thankachan
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
James T. McKenna
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
James M. McNally
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Chun Yang
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jee Hyun Choi
cCenter for Neuroscience, Korea Institute of Science and Technology, 130-722 Seoul, South Korea;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lichao Chen
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Bernat Kocsis
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
dDepartment of Psychiatry, Beth Israel Deaconess Medical Center, Boston, MA 02215; and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Karl Deisseroth
Departments of ePsychiatry and Behavioral Sciences and
fBioengineering, Stanford University, Stanford, CA 94305
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert E. Strecker
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Radhika Basheer
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ritchie E. Brown
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Ritchie E. Brown
Robert W. McCarley
aDepartment of Psychiatry, VA Boston Healthcare System, Brockton, MA 02301;
bDepartment of Psychiatry, Harvard Medical School, Boston, MA 02115;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: robert_mccarley@hms.harvard.edu
  1. Edited by Nancy Kopell, Boston University, Boston, MA, and approved February 2, 2015 (received for review July 17, 2014)

This article has a Correction. Please see:

  • Correction for Kim et al., Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations - April 27, 2015
  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Significance

When we are awake, purposeful thinking and behavior require the synchronization of brain cells involved in different aspects of the same task. Cerebral cortex electrical oscillations in the gamma (30–80 Hz) range are particularly important in such synchronization. In this report we identify a particular subcortical cell type which has increased activity during waking and is involved in activating the cerebral cortex and generating gamma oscillations, enabling active cortical processing. Abnormalities of the brain mechanisms controlling gamma oscillations are involved in the disordered thinking typical of neuropsychiatric disorders such as schizophrenia. Thus, these findings may pave the way for targeted therapies to treat schizophrenia and other disorders involving abnormal cortical gamma oscillations.

Abstract

Cortical gamma band oscillations (GBO, 30–80 Hz, typically ∼40 Hz) are involved in higher cognitive functions such as feature binding, attention, and working memory. GBO abnormalities are a feature of several neuropsychiatric disorders associated with dysfunction of cortical fast-spiking interneurons containing the calcium-binding protein parvalbumin (PV). GBO vary according to the state of arousal, are modulated by attention, and are correlated with conscious awareness. However, the subcortical cell types underlying the state-dependent control of GBO are not well understood. Here we tested the role of one cell type in the wakefulness-promoting basal forebrain (BF) region, cortically projecting GABAergic neurons containing PV, whose virally transduced fibers we found apposed cortical PV interneurons involved in generating GBO. Optogenetic stimulation of BF PV neurons in mice preferentially increased cortical GBO power by entraining a cortical oscillator with a resonant frequency of ∼40 Hz, as revealed by analysis of both rhythmic and nonrhythmic BF PV stimulation. Selective saporin lesions of BF cholinergic neurons did not alter the enhancement of cortical GBO power induced by BF PV stimulation. Importantly, bilateral optogenetic inhibition of BF PV neurons decreased the power of the 40-Hz auditory steady-state response, a read-out of the ability of the cortex to generate GBO used in clinical studies. Our results are surprising and novel in indicating that this presumptively inhibitory BF PV input controls cortical GBO, likely by synchronizing the activity of cortical PV interneurons. BF PV neurons may represent a previously unidentified therapeutic target to treat disorders involving abnormal GBO, such as schizophrenia.

  • ArchT
  • arousal
  • auditory steady-state response
  • channelrhodopsin2
  • optogenetics

Footnotes

  • ↵1Present address: Department of Psychiatry, Kyung Hee University Hospital at Gangdong, 134-727 Seoul, Korea.

  • ↵2T.K. and S.T. contributed equally to this work.

  • ↵3R.E.B. and R.W.M. contributed equally to this work.

  • ↵4To whom correspondence should be addressed. Email: robert_mccarley{at}hms.harvard.edu.
  • Author contributions: T.K., S.T., J.T.M., J.M.M., C.Y., R.E.S., R.B., R.E.B., and R.W.M. designed research; T.K., S.T., J.T.M., J.M.M., C.Y., L.C., and R.B. performed research; K.D. contributed new reagents/analytic tools; T.K., S.T., J.T.M., J.M.M., C.Y., J.H.C., B.K., R.E.S., R.B., R.E.B., and R.W.M. analyzed data; and T.K., S.T., J.T.M., J.M.M., C.Y., B.K., R.E.S., R.B., R.E.B., and R.W.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1413625112/-/DCSupplemental.

Freely available online through the PNAS open access option.

View Full Text
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Basal forebrain parvalbumin neurons and EEG gamma
Tae Kim, Stephen Thankachan, James T. McKenna, James M. McNally, Chun Yang, Jee Hyun Choi, Lichao Chen, Bernat Kocsis, Karl Deisseroth, Robert E. Strecker, Radhika Basheer, Ritchie E. Brown, Robert W. McCarley
Proceedings of the National Academy of Sciences Mar 2015, 112 (11) 3535-3540; DOI: 10.1073/pnas.1413625112

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Basal forebrain parvalbumin neurons and EEG gamma
Tae Kim, Stephen Thankachan, James T. McKenna, James M. McNally, Chun Yang, Jee Hyun Choi, Lichao Chen, Bernat Kocsis, Karl Deisseroth, Robert E. Strecker, Radhika Basheer, Ritchie E. Brown, Robert W. McCarley
Proceedings of the National Academy of Sciences Mar 2015, 112 (11) 3535-3540; DOI: 10.1073/pnas.1413625112
Digg logo Reddit logo Twitter logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 112 (11)
Table of Contents

Submit

Sign up for Article Alerts

Article Classifications

  • Biological Sciences
  • Neuroscience

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Conclusions
    • Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Abstract depiction of a guitar and musical note
Science & Culture: At the nexus of music and medicine, some see disease treatments
Although the evidence is still limited, a growing body of research suggests music may have beneficial effects for diseases such as Parkinson’s.
Image credit: Shutterstock/agsandrew.
Scientist looking at an electronic tablet
Opinion: Standardizing gene product nomenclature—a call to action
Biomedical communities and journals need to standardize nomenclature of gene products to enhance accuracy in scientific and public communication.
Image credit: Shutterstock/greenbutterfly.
One red and one yellow modeled protein structures
Journal Club: Study reveals evolutionary origins of fold-switching protein
Shapeshifting designs could have wide-ranging pharmaceutical and biomedical applications in coming years.
Image credit: Acacia Dishman/Medical College of Wisconsin.
White and blue bird
Hazards of ozone pollution to birds
Amanda Rodewald, Ivan Rudik, and Catherine Kling talk about the hazards of ozone pollution to birds.
Listen
Past PodcastsSubscribe
Goats standing in a pin
Transplantation of sperm-producing stem cells
CRISPR-Cas9 gene editing can improve the effectiveness of spermatogonial stem cell transplantation in mice and livestock, a study finds.
Image credit: Jon M. Oatley.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Latest Articles
  • Archive

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490