Dataset Information

Optimal decoding of correlated neural population responses in the primate visual cortex.

ABSTRACT: Even the simplest environmental stimuli elicit responses in large populations of neurons in early sensory cortical areas. How these distributed responses are read out by subsequent processing stages to mediate behavior remains unknown. Here we used voltage-sensitive dye imaging to measure directly population responses in the primary visual cortex (V1) of monkeys performing a demanding visual detection task. We then evaluated the ability of different decoding rules to detect the target from the measured neural responses. We found that small visual targets elicit widespread responses in V1, and that response variability at distant sites is highly correlated. These correlations render most previously proposed decoding rules inefficient relative to one that uses spatially antagonistic center-surround summation. This optimal decoder consistently outperformed the monkey in the detection task, demonstrating the sensitivity of our techniques. Overall, our results suggest an unexpected role for inhibitory mechanisms in efficient decoding of neural population responses.

SUBMITTER: Chen Y

PROVIDER: S-EPMC1851689 | biostudies-literature | 2006 Nov

REPOSITORIES: biostudies-literature

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Optimal decoding of correlated neural population responses in the primate visual cortex.

Chen Yuzhi Y Geisler Wilson S WS Seidemann Eyal E

Nature neuroscience 20061022 11

Even the simplest environmental stimuli elicit responses in large populations of neurons in early sensory cortical areas. How these distributed responses are read out by subsequent processing stages to mediate behavior remains unknown. Here we used voltage-sensitive dye imaging to measure directly population responses in the primary visual cortex (V1) of monkeys performing a demanding visual detection task. We then evaluated the ability of different decoding rules to detect the target from the m ...[more]

PMID: 17057706

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Project description:Variability in cortical neuronal responses to sensory stimuli and in perceptual decision making performance is substantial. Moment-to-moment fluctuations in waking state or arousal can account for much of this variability. Yet, this variability is rarely characterized across the full spectrum of waking states, leaving the characteristics of the optimal state for sensory processing unresolved. Using pupillometry in concert with extracellular multiunit and intracellular whole-cell recordings, we found that the magnitude and reliability of visually evoked responses in primary visual cortex (V1) of awake, passively behaving male mice increase as a function of arousal and are largest during sustained locomotion periods. During these high-arousal, sustained locomotion periods, cortical neuronal membrane potential was at its most depolarized and least variable. Contrastingly, behavioral performance of mice on two distinct visual detection tasks was generally best at a range of intermediate arousal levels, but worst during high arousal with locomotion. These results suggest that large, reliable responses to visual stimuli in V1 occur at a distinct arousal level from that associated with optimal visual detection performance. Our results clarify the relation between neuronal responsiveness and the continuum of waking states, and suggest new complexities in the relation between primary sensory cortical activity and behavior.SIGNIFICANCE STATEMENT Cortical sensory processing strongly depends on arousal. In the mouse visual system, locomotion (associated with high arousal) has previously been shown to enhance the sensory responses of neurons in primary visual cortex (V1). Yet, arousal fluctuates on a moment-to-moment basis, even during quiescent periods. The characteristics of V1 sensory processing across the continuum of arousal are unclear. Furthermore, the arousal level corresponding to optimal visual detection performance is unknown. We show that the magnitude and reliability of sensory-evoked V1 responses are monotonic increasing functions of arousal, and largest during locomotion. Visual detection behavior, however, is suboptimal during high arousal with locomotion, and usually best during intermediate arousal. Our study provides a more complete picture of the dependence of V1 sensory processing on arousal.

Dataset Information

Optimal decoding of correlated neural population responses in the primate visual cortex.

Publications

Optimal decoding of correlated neural population responses in the primate visual cortex.

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