Article

Parvalbumin-Expressing Interneurons Linearly Transform Cortical Responses to Visual Stimuli

Computational Neurosciences Graduate Program, University of California San Diego, La Jolla, California 92093-0634, USA.
Neuron (Impact Factor: 15.05). 01/2012; 73(1):159-70. DOI: 10.1016/j.neuron.2011.12.013
Source: PubMed

ABSTRACT

The response of cortical neurons to a sensory stimulus is shaped by the network in which they are embedded. Here we establish a role of parvalbumin (PV)-expressing cells, a large class of inhibitory neurons that target the soma and perisomatic compartments of pyramidal cells, in controlling cortical responses. By bidirectionally manipulating PV cell activity in visual cortex we show that these neurons strongly modulate layer 2/3 pyramidal cell spiking responses to visual stimuli while only modestly affecting their tuning properties. PV cells' impact on pyramidal cells is captured by a linear transformation, both additive and multiplicative, with a threshold. These results indicate that PV cells are ideally suited to modulate cortical gain and establish a causal relationship between a select neuron type and specific computations performed by the cortex during sensory processing.

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    • "Consequently, it is possible that presumed PV+ interneurons were implicated in a dynamic control of sensory cortical processing by POm. Other studies have demonstrated that PV+ interneurons participate in control gain of sensory responses[86,91,92]. Furthermore, recent findings demonstrate that the conditional ablation of Cav 2.1 channel function from cortical PV+ interneurons alters GABA release from these cells, impairs their ability to constrain cortical pyramidal cell excitability[93]. "

    Full-text · Article · Jan 2016 · PLoS ONE
    • "In this view, the essential question is whether the suppression that an interneuron type provides is predominantly divisive or predominantly subtractive (Atallah et al., 2012; Lee et al., 2012; Wilson et al., 2012). This framework has been applied to visual cortex by several groups with seemingly conflicting results (Atallah et al., 2012, 2014; Lee et al., 2012, 2014; Wilson et al., 2012; El-Boustani and Sur, 2014; Xue et al., 2014), producing an ongoing debate regarding whether separate functions of division and subtraction can be assigned to different populations of interneuron and whether those assignments are fixed. Indeed, evidence from a variety of physiological and modeling studies has converged to produce clear predictions regarding which interneuron types will implement divisive versus subtractive suppression (Vu and Krasne, 1992; Miles et al., 1996; Hao et al., 2009; Jadi et al., 2012). "
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    ABSTRACT: Cortical function is regulated by a strikingly diverse array of local-circuit inhibitory neurons. We evaluated how optogenetically activating somatostatin- and parvalbumin-positive interneurons subtractively or divisively suppressed auditory cortical cells' responses to tones. In both awake and anesthetized animals, we found that activating either family of interneurons produced mixtures of divisive and subtractive effects and that simultaneously recorded neurons were often suppressed in qualitatively different ways. A simple network model shows that threshold nonlinearities can interact with network activity to transform subtractive inhibition of neurons into divisive inhibition of networks, or vice versa. Varying threshold and the strength of suppression of a model neuron could determine whether the effect of inhibition appeared divisive, subtractive, or both. We conclude that the characteristics of response inhibition specific to a single interneuron type can be "masked" by the network configuration and cellular properties of the network in which they are embedded.
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    • "Based on these properties, fast-spiking, PV+ interneurons establish a temporal matrix for complex neuronal information processing (Fig. 1). Fast-spiking, PV+ interneurons also control pyramidal cell activity during gamma oscillations in the neocortex in vitro and in vivo (Atallah et al., 2012; Cardin et al., 2009; Cunningham et al., 2004; Galarreta and Hestrin, 1999, 2002; Sohal et al., 2009). Pyramidal cells, in contrast, show strong action potential frequency accommodation and have typical spiking rates around 1–3 Hz during hippocampal gamma oscillations in vitro and in vivo (Csicsvari et al., 2003; Gloveli et al., 2005; Hájos et al., 2004; Hájos and Paulsen, 2009). "
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    ABSTRACT: Fast-spiking, inhibitory interneurons - prototype is the parvalbumin-positive (PV+) basket cell - generate action potentials at high frequency and synchronize the activity of numerous excitatory principal neurons, such as pyramidal cells, during fast network oscillations by rhythmic inhibition. For this purpose, fast-spiking, PV+ interneurons have unique electrophysiological characteristics regarding action potential kinetics and ion conductances, which are associated with high energy expenditure. This is reflected in the neural ultrastructure by enrichment with mitochondria and cytochrome c oxidase, indicating the dependence on oxidative phosphorylation for adenosine-5'-triphosphate (ATP) generation. The high energy expenditure is most likely required for membrane ion transport in dendrites and the extensive axon arbor as well as for presynaptic release of neurotransmitter, gamma-aminobutyric acid (GABA). Fast-spiking, PV+ interneurons are central for the emergence of gamma oscillations (30-100Hz) that provide a fundamental mechanism of complex information processing during sensory perception, motor behavior and memory formation in networks of the hippocampus and the neocortex. Conversely, shortage in glucose and oxygen supply (metabolic stress) and/or excessive formation of reactive oxygen and nitrogen species (oxidative stress) may render these interneurons to be a vulnerable target. Dysfunction in fast-spiking, PV+ interneurons might set a low threshold for impairment of fast network oscillations and thus higher brain functions. This pathophysiological mechanism might be highly relevant for cerebral ageing as well as various acute and chronic brain diseases, such as stroke, vascular cognitive impairment, epilepsy, Alzheimer's disease and schizophrenia. Copyright © 2015. Published by Elsevier Inc.
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