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: 15.98). 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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    • "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; DOI:10.1016/j.neuron.2015.06.035 · 15.98 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 · 15.98 Impact Factor
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    • "In PV neuron clusters, the untuned responses of the insiders might be suppressed by inhibitory actions of clusters more effectively than the tuned responses, and consequently the OSI value was changed while the tuning width was not. This view seems consistent with the linear-threshold model in which the activation/suppression of PV neurons linearly scales responsiveness of nearby pyramidal cells, and thus the tuning width of the nearby cells is expected to change only when the PV neurons strongly suppress the untuned responses to baseline (Atallah et al., 2012). In SOM neurons , on the other hand, the amplitudes of the tuned response at the side of the optimal stimuli might be more preferentially suppressed by the inhibitory action of the clusters, and thus both tuning width and OSI were affected. "
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    ABSTRACT: Neocortical neurons with similar functional properties assemble into spatially coherent circuits, but it remains unclear how inhibitory interneurons are organized. We applied in vivo two-photon functional Ca(2+) imaging and whole-cell recording of synaptic currents to record visual responses of cortical neurons and analyzed their spatial arrangements. GABAergic interneurons were clustered in the 3D space of the mouse visual cortex, and excitatory neurons located within the clusters (insiders) had a lower amplitude and sharper orientation tuning of visual responses than outsiders. Inhibitory synaptic currents recorded from the insiders were larger than those of the outsiders. Single, isolated interneurons did not show such a location-tuning/amplitude relationship. The two principal subtypes of interneurons, parvalbumin- and somatostatin-expressing neurons, also formed clusters with only slightly overlapping each other and exhibited a different location-tuning relationship. These findings suggest that GABAergic interneurons and their subgroups form clusters to make their inhibitory function more effective than isolated interneurons. Copyright © 2014 The Authors. Published by Elsevier Inc. All rights reserved.
    Cell Reports 11/2014; In press(5). DOI:10.1016/j.celrep.2014.10.057 · 8.36 Impact Factor
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