Parallel processing by cortical inhibition enables context-dependent behavior

Kuchibhotla, Kishore V.; Gill, Jonathan V.; Lindsay, Grace W.; Papadoyannis, Eleni S.; Field, Rachel E.; Sten, Tom Hindmarsh; Miller, Kenneth D.; Froemke, Robert C.

doi:10.1038/nn.4436

Cited by 343 publications

(389 citation statements)

References 61 publications

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“…Third, stimulus-specific reduced firing rates among SOMs may disinhibit PVs relative to pyramidal neurons, leading to increased inhibition. Fourth, SOMs may relay a top-down or modulatory signal generated elsewhere that drives greater inhibition in specific stimulus contexts (Kuchibhotla et al, 2017; Pi et al, 2013). Testing each of these possibilities is required to disambiguate the specifics of the synaptic changes over the time scale of adaptation.…”

Section: Discussionmentioning

confidence: 99%

Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation

2017

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Neuronal stimulus selectivity is shaped by feedforward and recurrent excitatory-inhibitory interactions. In the auditory cortex (AC), parvalbumin- (PVs) and somatostatin-positive (SOMs) inhibitory interneurons differentially modulate frequency-dependent responses of excitatory neurons. Responsiveness of neurons in AC to sounds is furthermore dependent on stimulus history. We found that inhibitory effects of SOMs and PVs diverged as a function of adaptation to temporal repetition of tones. Prior to adaptation, suppressing either SOM or PV inhibition drove both increases and decreases in excitatory spiking activity. After adaptation, suppressing SOM activity caused predominantly disinhibitory effects, whereas suppressing PV activity still evoked bi-directional changes. SOM, but not PV-driven inhibition, dynamically modulated frequency tuning with adaptation. Unlike PV-driven, SOM-driven inhibition elicited gain-like increases in frequency tuning reflective of adaptation. Our findings suggest that distinct cortical interneurons differentially shape tuning to sensory stimuli across the neuronal receptive field, altering frequency selectivity of excitatory neurons during adaptation.

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Section: Discussionmentioning

confidence: 99%

Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation

2017

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“…Vice versa, the behavioral state affects circuit computations as well as long-range corticocortical interactions (Massimini et al, 2005; Ferrarelli et al, 2010; Fu et al, 2014; Kuchibhotla et al, 2017). The effects described here might have been modulated by urethane anesthesia that influences excitatory and inhibitory neuronal firing (Hara and Harris, 2002) and, consequently, might differ from multisensory interactions in the awake state (Iurilli et al, 2012; Ibrahim et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Rate and Temporal Coding Convey Multisensory Information in Primary Sensory Cortices

Bieler

Sieben

Cichon

et al. 2017

eNeuro

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Optimal behavior and survival result from integration of information across sensory systems. Modulation of network activity at the level of primary sensory cortices has been identified as a mechanism of cross-modal integration, yet its cellular substrate is still poorly understood. Here, we uncover the mechanisms by which individual neurons in primary somatosensory (S1) and visual (V1) cortices encode visual-tactile stimuli. For this, simultaneous extracellular recordings were performed from all layers of the S1 barrel field and V1 in Brown Norway rats in vivo and units were clustered and assigned to pyramidal neurons (PYRs) and interneurons (INs). We show that visual-tactile stimulation modulates the firing rate of a relatively low fraction of neurons throughout all cortical layers. Generally, it augments the firing of INs and decreases the activity of PYRs. Moreover, bimodal stimulation shapes the timing of neuronal firing by strengthening the phase-coupling between neuronal discharge and theta–beta band network oscillations as well as by modulating spiking onset. Sparse direct axonal projections between neurons in S1 and V1 seem to time the spike trains between the two cortical areas and, thus, may act as a substrate of cross-modal modulation. These results indicate that few cortical neurons mediate multisensory effects in primary sensory areas by directly encoding cross-modal information by their rate and timing of firing.

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“…For subsequent stable storage of learned information, the balance between excitation and inhibition must be restored. One means by which this balance is achieved is via compensatory inhibitory synaptic potentiation (6,22) (Fig. 1).…”

Section: Evidence For Restoration Of Ei Balance Through Inhibitory Symentioning

confidence: 99%

Inhibitory engrams in perception and memory

Barron

Vogels

Behrens

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

131

126

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Nervous systems use excitatory cell assemblies to encode and represent sensory percepts. Similarly, synaptically connected cell assemblies or "engrams" are thought to represent memories of past experience. Multiple lines of recent evidence indicate that brain systems create and use inhibitory replicas of excitatory representations for important cognitive functions. Such matched "inhibitory engrams" can form through homeostatic potentiation of inhibition onto postsynaptic cells that show increased levels of excitation. Inhibitory engrams can reduce behavioral responses to familiar stimuli, thereby resulting in behavioral habituation. In addition, by preventing inappropriate activation of excitatory memory engrams, inhibitory engrams can make memories quiescent, stored in a latent form that is available for contextrelevant activation. In neural networks with balanced excitatory and inhibitory engrams, the release of innate responses and recall of associative memories can occur through focused disinhibition. Understanding mechanisms that regulate the formation and expression of inhibitory engrams in vivo may help not only to explain key features of cognition but also to provide insight into transdiagnostic traits associated with psychiatric conditions such as autism, schizophrenia, and posttraumatic stress disorder.Percepts are thought to be represented in the brain by excitatory activity in groups of neurons, described as cell assemblies (1). Memories may similarly be represented by excitatory connections across different cell assemblies, which form when experiences trigger coordinated activity. Several recent studies indicate that the storage and reactivation of these excitatory "engrams" (2), respectively, may be accompanied by creation and modulation of matched inhibitory engrams. Here, we propose that inhibitory engrams, also termed "negative images" or "inhibitory representations," explain two fundamental features of animal and human psychology: first, behavioral habituation, which allows organisms to ignore familiar, frequently encountered percepts or stimuli, and, second, latent memory, wherein the brain stores tens of thousands of memories in a silent or latent state until recall is required. Such inhibitory engrams can be constructed in neural networks through simple, evolutionarily primitive, synaptic and cellular mechanisms, which are recognized to be involved in the phenomenon of excitatory-inhibitory (EI) balance observed across the brain.Neurons and neural circuits normally operate within a preset range of activity. Outside this range, altered levels of neuronal spiking trigger a variety of homeostatic mechanisms ranging from compensatory ion channel expression to local synaptic scaling (3, 4). These homeostatic mechanisms ensure that the activity parameters of a neuron operate around a set point such that the spiking rates remain stable and a balance of depolarizing and hyperpolarizing currents is maintained. As a consequence, excitation and inhibition are both locally and globally balanced, despite...

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Parallel processing by cortical inhibition enables context-dependent behavior

Cited by 343 publications

References 61 publications

Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation

Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation

Rate and Temporal Coding Convey Multisensory Information in Primary Sensory Cortices

Inhibitory engrams in perception and memory

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