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Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits

Abstract

Attention is a critical component of perception1. However, the mechanisms by which attention modulates neuronal communication to guide behaviour are poorly understood. To elucidate the synaptic mechanisms of attention, we developed a sensitive assay of attentional modulation of neuronal communication. In alert monkeys performing a visual spatial attention task, we probed thalamocortical communication by electrically stimulating neurons in the lateral geniculate nucleus of the thalamus while simultaneously recording shock-evoked responses from monosynaptically connected neurons in primary visual cortex. We found that attention enhances neuronal communication by increasing the efficacy of presynaptic input in driving postsynaptic responses, by increasing synchronous responses among ensembles of postsynaptic neurons receiving independent input, and by decreasing redundant signals between postsynaptic neurons receiving common input. The results demonstrate that attention finely tunes neuronal communication at the synaptic level by selectively altering synaptic weights, enabling enhanced detection of salient events in the noisy sensory environment.

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Figure 1: Attention task and behavioural performance.
Figure 2: Attentional modulation of thalamocortical synaptic efficacy.
Figure 3: Temporal precision of attentional enhancement of synaptic efficacy.
Figure 4: Attentional modulation of synchronized spiking.

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Acknowledgements

We thank K. E. Neverkovec, D. J. Sperka and R. Oates-O’Brien for technical and veterinary assistance. This work was supported by National Institutes of Health grants EY18683 (F.B.), EY013588 (W.M.U.), MH055714 (G.R.M.) and NSF grants BCS-0727115 and 1228535 (G.R.M. and W.M.U.).

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F.B., G.R.M. and W.M.U. designed the experiments. F.B. conducted the experiments and performed the data analyses in collaboration with G.R.M. and W.M.U. F.B., G.R.M. and W.M.U. wrote the manuscript.

Corresponding author

Correspondence to W. Martin Usrey.

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The authors declare no competing financial interests.

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Briggs, F., Mangun, G. & Usrey, W. Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits. Nature 499, 476–480 (2013). https://doi.org/10.1038/nature12276

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