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Impact Factor

Original Research ARTICLE

Front. Hum. Neurosci., 22 November 2010 | http://dx.doi.org/10.3389/fnhum.2010.00198

Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by low-threshold spiking and fast-spiking interneurons

  • 1 McGovern Institute of Brain Research, Massachusetts Institute of Technology, Cambridge, MA, USA
  • 2 Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, USA
  • 3 Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA

Selective optogenetic drive of fast-spiking (FS) interneurons (INs) leads to enhanced local field potential (LFP) power across the traditional “gamma” frequency band (20–80 Hz; Cardin et al., 2009). In contrast, drive to regular-spiking (RS) pyramidal cells enhances power at lower frequencies, with a peak at 8 Hz. The first result is consistent with previous computational studies emphasizing the role of FS and the time constant of GABAA synaptic inhibition in gamma rhythmicity. However, the same theoretical models do not typically predict low-frequency LFP enhancement with RS drive. To develop hypotheses as to how the same network can support these contrasting behaviors, we constructed a biophysically principled network model of primary somatosensory neocortex containing FS, RS, and low-threshold spiking (LTS) INs. Cells were modeled with detailed cell anatomy and physiology, multiple dendritic compartments, and included active somatic and dendritic ionic currents. Consistent with prior studies, the model demonstrated gamma resonance during FS drive, dependent on the time constant of GABAA inhibition induced by synchronous FS activity. Lower-frequency enhancement during RS drive was replicated only on inclusion of an inhibitory LTS population, whose activation was critically dependent on RS synchrony and evoked longer-lasting inhibition. Our results predict that differential recruitment of FS and LTS inhibitory populations is essential to the observed cortical dynamics and may provide a means for amplifying the natural expression of distinct oscillations in normal cortical processing.

Keywords: gamma, GABA, channelrhodopsin, low-threshold spiking, fast-spiking, interneurons, somatosensory cortex

Citation: Vierling-Claassen D, Cardin JA, Moore CI and Jones SR (2010) Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by low-threshold spiking and fast-spiking interneurons. Front. Hum. Neurosci. 4:198. doi: 10.3389/fnhum.2010.00198

Received: 01 June 2010; Accepted: 29 September 2010;
Published online: 22 November 2010.

Edited by:

Thilo Womelsdorf, Robarts Research Institute London, Canada

Reviewed by:

Gustavo Deco, Universitat Pompeu Fabra, Spain
Nancy J. Kopell, Boston University, USA

Copyright: © 2010 Vierling-Claassen, Cardin, Moore and Jones. This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

*Correspondence: Stephanie R. Jones, Athinoula A. Martinos Center for Biomedical Imaging, 149 Thirteenth Street, Suite 2301, Charlestown, MA 02129, USA. e-mail: srjones@nmr.mgh.harvard.edu