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Driving fast-spiking cells induces gamma rhythm and controls sensory responses

Cortical gamma oscillations (20-80 Hz) predict increases in focused attention, and failure in gamma regulation is a hallmark of neurological and psychiatric disease. Current theory predicts that gamma oscillations are generated by synchronous activity of fast-spiking inhibitory interneurons, with th...

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Published in:Nature 2009-06, Vol.459 (7247), p.663-667
Main Authors: Deisseroth, Karl, Tsai, Li-Huei, Moore, Christopher I, Cardin, Jessica A, Carlén, Marie, Meletis, Konstantinos, Knoblich, Ulf, Zhang, Feng
Format: Article
Language:English
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Summary:Cortical gamma oscillations (20-80 Hz) predict increases in focused attention, and failure in gamma regulation is a hallmark of neurological and psychiatric disease. Current theory predicts that gamma oscillations are generated by synchronous activity of fast-spiking inhibitory interneurons, with the resulting rhythmic inhibition producing neural ensemble synchrony by generating a narrow window for effective excitation. We causally tested these hypotheses in barrel cortex in vivo by targeting optogenetic manipulation selectively to fast-spiking interneurons. Here we show that light-driven activation of fast-spiking interneurons at varied frequencies (8-200 Hz) selectively amplifies gamma oscillations. In contrast, pyramidal neuron activation amplifies only lower frequency oscillations, a cell-type-specific double dissociation. We found that the timing of a sensory input relative to a gamma cycle determined the amplitude and precision of evoked responses. Our data directly support the fast-spiking-gamma hypothesis and provide the first causal evidence that distinct network activity states can be induced in vivo by cell-type-specific activation. Sensory transmission Gamma oscillations, synchronous activity rhythms in the neuronal network measured between 20 and 80 Hz, are active during information processing and attention, and are dysregulated in schizophrenia. What induces this activity band has been the subject of speculation and theory. Two papers in this issue report the use of cell-type-targeted optogenetic technologies to test the currently favoured theory — that these oscillations are generated by synchronous activity of fast-spiking (FS) interneurons, also known as parvalbumin-expressing interneurons. The results suggest that the theory is correct. Cardin et al . show that a gamma state can be driven by specific activation of FS interneurons in vivo , and that sensory input relative to these oscillations can determine the extent of evoked cortical activity. Sohal et al . report empirical evidence for the involvement of specific activation of FS interneurons in the production of gamma oscillations, and their data too suggest that gamma-based modulation of excitatory cells may enhance the signal-to-noise ratio in circuits. Cortical gamma oscillations (20–80 Hz) predict increases in focused attention, and failure in gamma regulation is a hallmark of neurological and psychiatric disease; however, what induces this activity band is unclear. Here, by using
ISSN:0028-0836
1476-4687
1476-4679
DOI:10.1038/nature08002