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


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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    • "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.
    Neurobiology of Disease 08/2015; DOI:10.1016/j.nbd.2015.08.005 · 5.08 Impact Factor
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    • "What candidate circuit mechanisms might underlie the multiplicative and additive fluctuations described here? A possibility lies in different interneuron classes: activation and inactivation of parvalbumin-or somatostatin-positive interneurons have been variously suggested to have multiplicative, additive, and combined (affine) effects on the firing rates of pyramidal cells (Atallah et al., 2012; Lee et al., 2012; Wilson et al., 2012). Another possibility lies in top-down connections from higher order cortices and thalamus. "
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    ABSTRACT: Neuronal responses of sensory cortex are highly variable, and this variability is correlated across neurons. To assess how variability reflects factors shared across a neuronal population, we analyzed the activity of many simultaneously recorded neurons in visual cortex. We developed a simple model that comprises two sources of shared variability: a multiplicative gain, which uniformly scales each neuron's sensory drive, and an additive offset, which affects different neurons to different degrees. This model captured the variability of spike counts and reproduced the dependence of pairwise correlations on neuronal tuning and stimulus orientation. The relative contributions of the additive and multiplicative fluctuations could vary over time and had marked impact on population coding. These observations indicate that shared variability of neuronal populations in sensory cortex can be largely explained by two factors that modulate the whole population. Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved.
    Neuron 07/2015; 87(3). DOI:10.1016/j.neuron.2015.06.035 · 15.05 Impact Factor
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    • "Recurrent excitation in rodents may be weaker than in species with columnar organization, so that excitatory instability and the transition to sublinear behavior may not occur. This is suggested by results of Atallah et al. (2012) in mouse V1 L2/3: optogenetic suppression of parvalbumin (PV)-expressing I cells increased E-cell visual responses without any increase in the excitatory conductance they received and with a nonparadoxical increase in inhibitory conductance, suggesting a dearth of E / E coupling and non-ISN behavior. This could explain why maps fail to develop in rodents, as such failure can occur if local interactions between neurons are suppressive (Kaschube, 2014). "
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    ABSTRACT: Neurons in sensory cortex integrate multiple influences to parse objects and support perception. Across multiple cortical areas, integration is characterized by two neuronal response properties: (1) surround suppression-modulatory contextual stimuli suppress responses to driving stimuli; and (2) "normalization"-responses to multiple driving stimuli add sublinearly. These depend on input strength: for weak driving stimuli, contextual influences facilitate or more weakly suppress and summation becomes linear or supralinear. Understanding the circuit operations underlying integration is critical to understanding cortical function and disease. We present a simple, general theory. A wealth of integrative properties, including the above, emerge robustly from four cortical circuit properties: (1) supralinear neuronal input/output functions; (2) sufficiently strong recurrent excitation; (3) feedback inhibition; and (4) simple spatial properties of intracortical connections. Integrative properties emerge dynamically as circuit properties, with excitatory and inhibitory neurons showing similar behaviors. In new recordings in visual cortex, we confirm key model predictions. Copyright © 2015 Elsevier Inc. All rights reserved.
    Neuron 01/2015; 85(2):402-17. DOI:10.1016/j.neuron.2014.12.026 · 15.05 Impact Factor
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