Attention Induced Gain Stabilization in Broad and Narrow-Spiking Cells in the Frontal Eye-Field of Macaque Monkeys

TY - JOUR

T1 - Attention Induced Gain Stabilization in Broad and Narrow-Spiking Cells in the Frontal Eye-Field of Macaque Monkeys

AU - Thiele, Alexander

AU - Brandt, Christian

AU - Dasilva, Miguel

AU - Gotthardt, Sascha

AU - Chicharro, Daniel

AU - Panzeri, Stefano

AU - Distler, Claudia

N1 - Copyright © 2016 Thiele et al.

PY - 2016/7/20

Y1 - 2016/7/20

N2 - UNLABELLED: Top-down attention increases coding abilities by altering firing rates and rate variability. In the frontal eye field (FEF), a key area enabling top-down attention, attention induced firing rate changes are profound, but its effect on different cell types is unknown. Moreover, FEF is the only cortical area investigated in which attention does not affect rate variability, as assessed by the Fano factor, suggesting that task engagement affects cortical state nonuniformly. We show that putative interneurons in FEF of Macaca mulatta show stronger attentional rate modulation than putative pyramidal cells. Partitioning rate variability reveals that both cell types reduce rate variability with attention, but more strongly so in narrow-spiking cells. The effects are captured by a model in which attention stabilizes neuronal excitability, thereby reducing the expansive nonlinearity that links firing rate and variance. These results show that the effect of attention on different cell classes and different coding properties are consistent across the cortical hierarchy, acting through increased and stabilized neuronal excitability.SIGNIFICANCE STATEMENT: Cortical processing is critically modulated by attention. A key feature of this influence is a modulation of "cortical state," resulting in increased neuronal excitability and resilience of the network against perturbations, lower rate variability, and an increased signal-to-noise ratio. In the frontal eye field (FEF), an area assumed to control spatial attention in human and nonhuman primates, firing rate changes with attention occur, but rate variability, quantified by the Fano factor, appears to be unaffected by attention. Using recently developed analysis tools and models to quantify attention effects on narrow- and broad-spiking cell activity, we show that attention alters cortical state strongly in the FEF, demonstrating that its effect on the neuronal network is consistent across the cortical hierarchy.

AB - UNLABELLED: Top-down attention increases coding abilities by altering firing rates and rate variability. In the frontal eye field (FEF), a key area enabling top-down attention, attention induced firing rate changes are profound, but its effect on different cell types is unknown. Moreover, FEF is the only cortical area investigated in which attention does not affect rate variability, as assessed by the Fano factor, suggesting that task engagement affects cortical state nonuniformly. We show that putative interneurons in FEF of Macaca mulatta show stronger attentional rate modulation than putative pyramidal cells. Partitioning rate variability reveals that both cell types reduce rate variability with attention, but more strongly so in narrow-spiking cells. The effects are captured by a model in which attention stabilizes neuronal excitability, thereby reducing the expansive nonlinearity that links firing rate and variance. These results show that the effect of attention on different cell classes and different coding properties are consistent across the cortical hierarchy, acting through increased and stabilized neuronal excitability.SIGNIFICANCE STATEMENT: Cortical processing is critically modulated by attention. A key feature of this influence is a modulation of "cortical state," resulting in increased neuronal excitability and resilience of the network against perturbations, lower rate variability, and an increased signal-to-noise ratio. In the frontal eye field (FEF), an area assumed to control spatial attention in human and nonhuman primates, firing rate changes with attention occur, but rate variability, quantified by the Fano factor, appears to be unaffected by attention. Using recently developed analysis tools and models to quantify attention effects on narrow- and broad-spiking cell activity, we show that attention alters cortical state strongly in the FEF, demonstrating that its effect on the neuronal network is consistent across the cortical hierarchy.

KW - Action Potentials/physiology

KW - Analysis of Variance

KW - Animals

KW - Attention/physiology

KW - Brain Mapping

KW - Cues

KW - Fixation, Ocular

KW - Fourier Analysis

KW - Macaca mulatta

KW - Neurons/cytology

KW - Photic Stimulation

KW - Visual Cortex/cytology

KW - Visual Fields/physiology

U2 - 10.1523/JNEUROSCI.0872-16.2016

DO - 10.1523/JNEUROSCI.0872-16.2016

M3 - SCORING: Journal article

C2 - 27445139

VL - 36

SP - 7601

EP - 7612

JO - J NEUROSCI

JF - J NEUROSCI

SN - 0270-6474

IS - 29

ER -