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Attention induces synchronization-based response gain in steady-state visual evoked potentials

Abstract

When attention is voluntarily directed to a spatial location, visual sensitivity increases at that location. What causes this improved sensitivity? Studies of single neuron spike rates in monkeys have provided mixed results in regard to whether attending to a stimulus increases its effective contrast (contrast gain) or multiplicatively boosts stimulus-driven neural responses (response or activity gain). We monitored frequency-tagged steady-state visual evoked potentials (SSVEPs) in humans and found that voluntary sustained attention multiplicatively increased stimulus-driven population electrophysiological activity. Analyses of intertrial phase coherence showed that this attentional response gain was at least partially due to the increased synchronization of SSVEPs to stimulus flicker. These results suggest that attention operates in a complementary manner at different levels; attention seems to increase single-neuron spike rates in a variety of ways, including contrast, response and activity gains, while also inducing a multiplicative boost on neural population activity via enhanced response synchronization.

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Figure 1: The contrast, response and activity gain hypotheses of the way voluntary visual-spatial attention boosts neural responses.
Figure 2: Stimuli and a trial sequence.
Figure 3: Topographic plots of the second-harmonic SSVEPs in response to the two gratings, averaged across observers and stimulus contrasts.
Figure 4: Second-harmonic SSVEP contrast-response functions.
Figure 5: Representative simulation results indicate that an attentional response or activity gain effect could not emerge from averaging neuronal contrast gain effects over a population of neurons with a variety of contrast-response functions and contrast gain magnitudes.
Figure 6: ITPC for second-harmonic SSVEPs averaged across contralateral focal electrodes, which are illustrated in Figure 4a.
Figure 7: Contrast dependence of ITPC for second-harmonic SSVEPs (averaged across contralateral focal electrodes, see Fig. 4a) when gratings were attended versus ignored.
Figure 8: Examples of probe displays for the control experiment.

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Acknowledgements

This work was supported by a US National Institutes of Health Grant EY14110 to S.S. and by National Institutes of Health Grant NS34639 and US National Science Foundation Grant BCS0518800 to K.A.P.

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Correspondence to Satoru Suzuki.

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Joon Kim, Y., Grabowecky, M., Paller, K. et al. Attention induces synchronization-based response gain in steady-state visual evoked potentials. Nat Neurosci 10, 117–125 (2007). https://doi.org/10.1038/nn1821

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