Scientific Understanding of Consciousness
Focused Attention -- Gamma Oscillations (20-80 Hz)
Nature 459, 663-667 (4 June 2009)
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Jessica A. Cardin, Marie Carlén, Konstantinos Meletis, Ulf Knoblich, Feng Zhang, Karl Deisseroth, Li-Huei Tsai & Christopher I. Moore
McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts 02139, USA
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA
Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts 02139, USA
Stanley Center for Psychiatric Research, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA
Department of Bioengineering, Stanford University, Stanford, California 94305, USA
Howard Hughes Medical Institute, Cambridge, Massachusetts 02139, USA
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.
Brain states characterized by rhythmic electrophysiological activity have been studied intensively for more than 80 years. Because these brain rhythms are believed to be essential to information processing, many theories have been proposed to explain their origin, with several emphasizing the activity of neural subtypes. One of the strongest cases made so far for the importance of a specific cell type in rhythm induction is the suggested role of fast-spiking (FS) interneurons in gamma oscillations. Networks of FS cells connected by gap junctions provide large, synchronous inhibitory postsynaptic potentials (IPSPs) to local excitatory neurons. Computational modelling indicates that this synchronous activity is sufficient to induce 20-80-Hz oscillations that are stabilized and regulated by fast excitatory feedback from pyramidal neurons. Cortical recordings in vivo show sensory-evoked gamma oscillations in the local field potential (LFP) and phase-locked firing of excitatory pyramidal cells, indicating entrainment of excitatory neurons to rhythmic inhibitory activity.
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