Attention Enhances the Efficacy of Communication in V1 Local Circuits

Abstract

Attention is a critical component of visual perception; however, the mechanisms of attention at the granular level are poorly understood. One possible mechanism by which attention modulates neuronal activity is to control the efficacy of communication between connected neurons; however, it is unclear whether attention alters communication efficacy across a variety of neuronal circuits. In parallel, attentional modulation of neuronal firing rate is not uniform but depends upon the match between neuronal feature selectivity and the feature required for successful task completion. Here we tested whether modulation of communication efficacy is a viable mechanism of attention by assessing whether it is consistent across a variety of neuronal circuits and dependent upon the type of information conveyed in each circuit. We identified monosynaptically connected pairs of V1 neurons through cross-correlation of neuronal spike trains recorded in adult female macaque monkeys performing attention-demanding contrast-change detection tasks. Attention toward the stimulus in the receptive field of recorded neurons significantly facilitated the efficacy of communication among connected pairs of V1 neurons. The amount of attentional enhancement depended upon neuronal physiology, with larger facilitation for circuits conveying information about task-relevant features. Furthermore, presynaptic activity was more determinant of attentional enhancement of communication efficacy than postsynaptic activity, and feedforward local circuits often displayed the largest facilitation with attention. Together, these findings highlight attentional modulation of communication efficacy as a generalized mechanism of attention and demonstrate that attentional modulation at the granular level depends on the relevance of feature-specific information conveyed by neuronal circuits.

Functional MRI and EEG Index Complementary Attentional Modulations

“…Therefore, this cannot account for the divergent observations between top-down attentional modulations of fMRI and early sensory evoked potentials measured by EEG. Instead, our data are consistent with a recent proposal suggesting spatial attention enhances synaptic efficacy between neurons in the early visual system (Briggs et al, 2013;Hembrook-Short et al, 2019). Such an increase in synaptic efficacy would increase local signaling, which can result in increased broadband LFPs, even at low (or 0%) contrasts.…”

Selection and suppression of visual information in the macaque prefrontal cortex

“…Spatial attention is hypothesized to act as a spatial filtering ‘in’ mechanism, that enhances the selection of incoming visual stimuli depending on their distance to its focus ( 22, 42, 43 ). This attention-based spatial filtering is often equated with spatial prioritization by cue instruction.…”

Changes in Local Network Activity Approximated by Reverse Spike-Triggered Local Field Potentials Predict the Focus of Attention

“…Prior work demonstrated that attention increases the likelihood that a presynaptic input generates a postsynaptic spike among connected pairs of neurons ( Briggs et al. 2013 ; Hembrook-Short et al. 2019 ).…”

“…In both geniculocortical circuits and local circuits within primary visual cortex (V1), attention significantly enhances the likelihood that a presynaptic input gives rise to a postsynaptic spike ( Briggs et al. 2013 ; Hembrook-Short et al. 2019 ).…”

“…2019 ). Although attention enhances synaptic efficacy for most connected pairs, local V1 circuits transmitting task-relevant feature information are enhanced more than those transmitting task-irrelevant signals ( Hembrook-Short et al. 2019 ).…”