Abstract
Cortical gain regulation allows neurons to respond adaptively to changing inputs. Neural gain is modulated by internal and external influences, including attentional and arousal states, motor activity and neuromodulatory input. These influences converge to a common set of mechanisms for gain modulation, including GABAergic inhibition, synaptically driven fluctuations in membrane potential, changes in cellular conductance and changes in other biophysical neural properties. Recent work has identified GABAergic interneurons as targets of neuromodulatory input and mediators of state-dependent gain modulation. Here, we review the engagement and effects of gain modulation in the cortex. We highlight key recent findings that link phenomenological observations of gain modulation to underlying cellular and circuit-level mechanisms. Finally, we place these cellular and circuit interactions in the larger context of their impact on perception and cognition.
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Acknowledgements
This work was supported by US National Institutes of Health (NIH) R01 MH102365, NIH R01 EY022951, NIH R01 MH113852, a Simons Foundation Autism Research Initiative (SFARI) Research Grant, a Smith Family Award for Excellence in Biomedical Research, a Klingenstein Fellowship Award, an Alfred P. Sloan Fellowship, a US National Alliance for Research on Schizophrenia & Depression (NARSAD) Young Investigator Award, a McKnight Fellowship and a grant from the Ludwig Family Foundation to J.A.C.; and a Brown-Coxe fellowship and a NARSAD Young Investigator Award to K.A.F. The authors thank M. J. Higley and members of the Cardin and Higley laboratories for insightful discussions, and Q. Perrenoud for help with illustration.
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Glossary
- Gain modulation
-
A phenomenon whereby the gain or sensitivity of a neuron to inputs, such as visual stimuli, is altered without changing selectivity.
- Input–output (I/O) relationship
-
The relationship between the inputs a neuron receives (such as synaptic inputs, direct currents or sensory stimulation) and the firing rate responses of that neuron.
- Synaptic summation
-
The summation of synaptic inputs to a neuron either spatially (when nearby synapses are coactive on a dendritic branch) or temporally (when synaptic inputs occur within a short time window mediated by the membrane time constant, τ).
- Iceberg effect
-
An effect whereby, if subthreshold responses to a stimulus are less selective than the neuron’s firing, a linear increase or decrease in activity may alter the neuron’s selectivity by raising or lowering the tuning curve of the neuron across the threshold.
- Monocular deprivation
-
An experimental paradigm in which an animal is deprived of vision from one eye during a critical developmental period. The mature binocular visual cortex then responds predominantly to inputs from the non-deprived eye.
- Stochastic resonance
-
A phenomenon in which the addition of noise non-linearly enhances the information content of a signal, by boosting resonant frequencies over a sensor’s detection threshold (such as a cell’s spike threshold).
- Shunting inhibition
-
A GABAergic synaptic input that minimally affects the membrane potential of a cell that is near the inhibitory synaptic reversal potential, but that leads to a reduction of nearby excitatory postsynaptic potential amplitudes.
- Pairwise correlations
-
A normalized measure of covariation between pairs of neurons that can give insight into their tuning similarity (signal correlations) or shared trial-to-trial variability (noise correlations).
- Dendritic saturation
-
A phenomenon in which an already depolarized dendritic branch shows reduced excitatory responses to temporally correlated excitatory inputs due to reduced driving force.
- Synaptic efficacy
-
The influence that a presynaptic input has on a postsynaptic cell’s probability of firing an action potential.
- Adaptation
-
A decrease in sensitivity to constant or repeated stimuli, leading to reduced stimulus-evoked neural responses over time.
- Forward suppression
-
A rapid form of sensory adaptation whereby the response to a stimulus is reduced when preceded by a stimulus with similar features.
- Feedback inhibition
-
A type of inhibition delivered through recurrent connections: that is, local inhibitory cells target the same population of excitatory cells that drive local inhibitory activity.
- Brain states
-
Spatiotemporal patterns of neural-network activity across the brain that are dynamically regulated by behaviour, the environment and the internal state.
- Pupil diameter
-
The diameter of the pupil of the eye. The diameter is tightly coupled to various emotional and cognitive factors, including global arousal and attention, even when controlling for changes in luminance and depth accommodation.
- Attractor dynamics
-
Temporal patterns that evolve towards a stable state from a large range of starting conditions. Attractor network characterization facilitates the identification of key network properties.
- Winner-take-all mechanism
-
A computational principle in which non-linearities in a recurrent neural network create strong competition between neurons. Only neurons (or sets thereof) with the strongest responses remain active, providing a mechanism for input selection or segregation.
- Dimensionality reduction
-
Reduction of the number of random variables of a system to a smaller set of principal variables to aid analysis.
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Ferguson, K.A., Cardin, J.A. Mechanisms underlying gain modulation in the cortex. Nat Rev Neurosci 21, 80–92 (2020). https://doi.org/10.1038/s41583-019-0253-y
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DOI: https://doi.org/10.1038/s41583-019-0253-y
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