Bottom-Up and Top-Down Input Augment the Variability of Cortical Neurons

Neurons in the cerebral cortex respond inconsistently to a repeated sensory stimulus, yet they underlie our stable sensory experiences. Although the nature of this variability is unknown, its ubiquity has encouraged the general view that each cell produces random spike patterns that noisily represen...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2016-08, Vol.91 (3), p.540-547
Main Authors: Gómez-Laberge, Camille, Smolyanskaya, Alexandra, Nassi, Jonathan J., Kreiman, Gabriel, Born, Richard T.
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
Cold Temperature
Macaca mulatta
Male
Models, Neurological
Neurons
Neurons - physiology
Neurosciences
Simulation
Visual Cortex - cytology
Visual Cortex - physiology
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Summary:Neurons in the cerebral cortex respond inconsistently to a repeated sensory stimulus, yet they underlie our stable sensory experiences. Although the nature of this variability is unknown, its ubiquity has encouraged the general view that each cell produces random spike patterns that noisily represent its response rate. In contrast, here we show that reversibly inactivating distant sources of either bottom-up or top-down input to cortical visual areas in the alert primate reduces both the spike train irregularity and the trial-to-trial variability of single neurons. A simple model in which a fraction of the pre-synaptic input is silenced can reproduce this reduction in variability, provided that there exist temporal correlations primarily within, but not between, excitatory and inhibitory input pools. A large component of the variability of cortical neurons may therefore arise from synchronous input produced by signals arriving from multiple sources. •Inactivation of corticocortical input reduces neuronal spiking variability•An integrate-and-fire model captures the effect when excitatory input is synchronized•Input heterogeneity plays a significant role in neuronal variability Even though models of neuronal firing have depicted neurons as intrinsically capricious, Gómez-Laberge et al. show that the irregular activity of neurons in macaque visual cortex is partially due to input from other cortical areas. A computational model suggests that long-range input may augment variability by synchronizing local excitation.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2016.06.028