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Attention-dependent reductions in burstiness and action-potential height in macaque area V4

Nature Neuroscience volume 16, pages 1125–1131 (2013)Cite this article

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Abstract

Attention improves the encoding of visual stimuli. One mechanism that is implicated in facilitating sensory encoding is the firing of action potentials in bursts. We tested the hypothesis that when spatial attention is directed to a stimulus, this causes an increase in burst firing to the attended stimulus. To the contrary, we found an attention-dependent reduction in 'burstiness' among putative pyramidal neurons in macaque area V4. We accounted for this using a conductance-based Hodgkin-Huxley style model in which attentional modulation stems from scaling excitation and inhibition. The model exhibited attention-dependent increases in firing rate and made the surprising and correct prediction that when attention is directed into a neuron's receptive field, this reduces action-potential height. The model thus provided a unified explanation for three distinct forms of attentional modulation, two of them previously undescribed, and implicates scaling of the responses of excitatory and inhibitory input populations in mediating attention.

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Figure 1: Attention-dependent reduction in the burstiness.
Figure 2: Scaled conductance model of attention.
Figure 3: Narrow-spiking neurons show less spike history–dependent height adaptation than do broad-spiking neurons.
Figure 4: Attention-dependent reduction in action-potential height.

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Change history

  • 17 July 2013

    In the version of this article initially published online, burstiness was defined on p. 1 as the prosperity of neurons to fire rather than the propensity, and model neuron firing rates were given on p. 3 in nHz rather than Hz. The errors have been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

This work was supported in part by US National Eye Institute grant EY13802 (J.F.M. and J.H.R.) and The Gatsby Charitable Foundation (E.B.A. and J.H.R.). We thank K. Sundberg for help in data collection, and C. Williams and J. Reyes for help with animal care.

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Authors and Affiliations

  1. The Salk Institute for Biological Studies, San Diego, California, USA

    Emily B Anderson, Jude F Mitchell & John H Reynolds

  2. Center for Integrative Neuroscience and Department of Physiology, University of California, San Francisco, San Francisco, California, USA

    Emily B Anderson

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  1. Emily B Anderson
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Contributions

E.B.A. analyzed the data and built the model. J.F.M. collected most of the physiology data and contributed to the burst-reduction analyses. E.B.A., J.F.M. and J.H.R. wrote the manuscript.

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Correspondence to Emily B Anderson or John H Reynolds.

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The authors declare no competing financial interests.

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Anderson, E., Mitchell, J. & Reynolds, J. Attention-dependent reductions in burstiness and action-potential height in macaque area V4. Nat Neurosci 16, 1125–1131 (2013). https://doi.org/10.1038/nn.3463

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