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Control of visual cortical signals by prefrontal dopamine

Abstract

The prefrontal cortex is thought to modulate sensory signals in posterior cortices during top-down attention1,2, but little is known about the underlying neural circuitry. Experimental and clinical evidence indicate that prefrontal dopamine has an important role in cognitive functions3, acting predominantly through D1 receptors. Here we show that dopamine D1 receptors mediate prefrontal control of signals in the visual cortex of macaques (Macaca mulatta). We pharmacologically altered D1-receptor-mediated activity in the frontal eye field of the prefrontal cortex and measured the effect on the responses of neurons in area V4 of the visual cortex. This manipulation was sufficient to enhance the magnitude, the orientation selectivity and the reliability of V4 visual responses to an extent comparable with the known effects of top-down attention. The enhancement of V4 signals was restricted to neurons with response fields overlapping the part of visual space affected by the D1 receptor manipulation. Altering either D1- or D2-receptor-mediated frontal eye field activity increased saccadic target selection but the D2 receptor manipulation did not enhance V4 signals. Our results identify a role for D1 receptors in mediating the control of visual cortical signals by the prefrontal cortex and suggest how processing in sensory areas could be altered in mental disorders involving prefrontal dopamine.

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Figure 1: Local manipulation of D1R-mediated activity in the FEF during single-neuron electrophysiology in area V4.
Figure 2: Manipulation of D1R-mediated activity enhances V4 visual signals.
Figure 3: Changes in saccadic target selection and V4 visual responses.

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Acknowledgements

We thank D. S. Aldrich for technical assistance, N. Steinmetz for help with Fano factor analysis and W. T. Newsome, E. I. Knudsen, K. M. Armstrong and R. F. Squire for comments on the manuscript. This work was supported by NIH EY014924, NSF IOB-0546891, The McKnight Foundation and an IBRO Fellowship to B.N.

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B.N. designed and performed experiments, analysed data and wrote the paper; T.M. designed and performed experiments and wrote the paper.

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Correspondence to Behrad Noudoost.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, a Supplementary Discussion, Supplementary Figures 1-7 with legends and additional references. (PDF 657 kb)

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Noudoost, B., Moore, T. Control of visual cortical signals by prefrontal dopamine. Nature 474, 372–375 (2011). https://doi.org/10.1038/nature09995

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