Parvalbumin neurons and gamma rhythms enhance cortical circuit performance

By V. Sohal, Feng Zhang, Feng Zhang, Ofer Yizhar, Karl Deisseroth. Nature, 2009

2,652 citations recorded by the source corpus.

Synchronized oscillations and inhibitory interneurons have important and interconnected roles within cortical microcircuits. In particular, interneurons defined by the fast-spiking phenotype and expression of the calcium-binding protein parvalbumin have been suggested to be involved in gamma (30–80 Hz) oscillations, which are hypothesized to enhance information processing. However, because parvalbumin interneurons cannot be selectively controlled, definitive tests of their functional significance in gamma oscillations, and quantitative assessment of the impact of parvalbumin interneurons and gamma oscillations on cortical circuits, have been lacking despite potentially enormous significance (for example, abnormalities in parvalbumin interneurons may underlie altered gamma-frequency synchronization and cognition in schizophrenia and autism). Here we use a panel of optogenetic technologies in mice to selectively modulate multiple distinct circuit elements in neocortex, alone or in combination. We find that inhibiting parvalbumin interneurons suppresses gamma oscillations in vivo, whereas driving these interneurons (even by means of non-rhythmic principal cell activity) is sufficient to generate emergent gamma-frequency rhythmicity. Moreover, gamma-frequency modulation of excitatory input in turn was found to enhance signal transmission in neocortex by reducing circuit noise and amplifying circuit signals, including inputs to parvalbumin interneurons. As demonstrated here, optogenetics opens the door to a new kind of informational analysis of brain function, permitting quantitative delineation of the functional significance of individual elements in the emergent operation and function of intact neural circuitry.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/c21bf2611aaaab720502f229395fb9fd00229349

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Citations in the corpus

Frontiers in Integrative Neuroscience Integrative Neuroscience Neural Synchrony in Cortical Networks: History, Concept and Current Status (neutral): “Through this additional function they assume a pivotal role in the temporal structuring and coordination of neuronal responses (Cardin et al., 2009; Sohal et al., 2009; for a review see Bartos et al., 2007).”
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition (2010, background): “Two groups reported that activating channorodopsin-2 (a cation channel) in fast spiking interneurons led to entrainment of pyramidal cells preferentially at gamma frequencies in mouse frontal (885) and somatosensory (155) cortex.”
The Development and Application of Optogenetics (2011, methodology): “This doublefloxed inverted open-reading-frame (DIO; reviewed in Zhang et al. 2010) strategy (Atasoy et al. 2008, Sohal et al. 2009, Tsai et al. 2009) situates the opsin gene (inhibitory or excitatory) in the inverted (meaningless) orientation, but the gene is flanked by two sets of incompatible Cre…”
How Inhibition Shapes Cortical Activity (2011, neutral): “Among the various types of inhibitory neurons , basket cells play a key role in gamma oscillations (Cardin et al., 2009; Cobb et al., 1995; Sohal et al., 2009).”
Modulation of visual responses by behavioral state in mouse visual cortex. (2010, positive): “It is worth noting that the increased responsiveness was accompanied by an increase in gamma-frequency oscillations; two recent studies have demonstrated that gamma oscillations mediated by parvalbumin-expressing interneurons can facilitate transmission of information in cortical circuits (Cardin et”
Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities and core autism-related deficits (2011, positive): “This was particularly important, as GABAergic interneurons are recognized as playing a crucial role in the precise timing of neuronal activity (Sohal et al., 2009) and there is increasing evidence of abnormal neural synchrony as a pathophysiological mechanism in ASD (Uhlhaas and Singer, 2006;…”
Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms (2013, positive): “These approaches can be enhanced by optogenetic identification of neurons and by their selective perturbation (Cardin et al., 2009; Sohal et al., 2009; Stark et al., 2012), complemented with high spatial-resolution imaging (Svoboda and Yasuda, 2006) and computational modeling (Wang, 2010) to aid in…”
Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins (2011, methodology): “We therefore sequentially (i) compared the properties of the ChETA mutants to identify the most promising, (ii) tested the performance of those ChETA mutants in eliciting high-frequency spikes in fast-spiking neurons in PvalbCcre mic”
The graphical brain: Belief propagation and active inference (2017, background): “These include synchronous gain (Chawla, Lumer, & Friston, 1999) that is thought to be mediated by interactions with inhibitory interneurons that are, themselves, replete with voltage-sensitive NMDA receptors (Lee et al., 2013; Sohal et al., 2009).”
Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition (2010, background): “It should be mentioned that GABAergic interneurons also have been strongly implicated in the generation of the much faster 30–100 Hz gamma rhythm (Traub et al., 1999; Bartos et al., 2007; Mann and Paulsen, 2007; Cardin et al., 2009; Sohal et al., 2009).”