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. 2011 May 15;474(7351):372-5.
doi: 10.1038/nature09995.

Control of Visual Cortical Signals by Prefrontal Dopamine

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Free PMC article

Control of Visual Cortical Signals by Prefrontal Dopamine

Behrad Noudoost et al. Nature. .
Free PMC article

Abstract

The prefrontal cortex is thought to modulate sensory signals in posterior cortices during top-down attention, but little is known about the underlying neural circuitry. Experimental and clinical evidence indicate that prefrontal dopamine has an important role in cognitive functions, 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.

Figures

Figure 1
Figure 1
Local manipulation of D1R-mediated activity within the FEF during single neuron electrophysiology in area V4. a, Lateral view of the macaque brain depicts the location of a recording microsyringe within the FEF and of recording sites within area V4. Bottom diagram shows saccades evoked via electrical microstimulation at the infusion site (red traces) and the RF (green ellipse) of a recorded V4 neuron in an example experiment. b, Double-target, saccade task used to measure the monkey’s tendency to make saccades to a target within the FEFRF vs. one at an opposite location across varying temporal onset asynchronies. Positive asynchrony values denote earlier onset of FEFRF targets. Bottom plot shows the leftward shift in the PES, indicating more FEFRF choices, following infusion of SCH23390 into an FEF site. c, Visual responses of a V4 neuron with a RF that overlapped the FEFRF measured during passive fixation. The plot shows mean±S.E.M. visual responses to a bar stimulus presented at orthogonal orientations before (gray) and after (red) the infusion of SCH23390 at the FEF site.
Figure 2
Figure 2
Manipulation of D1R-mediated activity enhances V4 visual signals. a, Average vectors of saccades evoked at all FEF sites that overlapped V4 RFs (left). Distribution of distances between the endpoint of evoked saccades and the centers of overlapping V4RFs for 37 V4 neurons. The mean normalized response magnitude (b), orientation selectivity (c) and response variability (FF) (d) of V4 neurons before (gray) and after (red) microinfusion of SCH23390 into the FEF. Shown are means ± S.E.M. within a 100-ms moving window measured during the 1-second RF stimulus presentation (top event plot). Histograms to the right of each response profile show the distributions of modulation indices for response magnitude (b), selectivity (c) and variability (d) across the population of neurons. e, Comparison of V4 response modulation following the SCH23390 infusion for preferred and non-preferred RF stimuli.
Figure 3
Figure 3
Changes in saccadic target selection and V4 visual responses. a, Scatter plot shows the consistent increase in FEFRF target choices (decrease in PES) after manipulation of both D1R (circles) and D2R-mediated (triangles) FEF activity. For both drug effects, the increase in FEFRF target selection was constant across a range of control PES values; the slope in the linear fit did not differ significantly from unity in either case (D1R: slope=0.96, p=0.552; D2R: slope=0.97, p=0.502). b, Changes in response magnitude, orientation selectivity and response variability (FF) following each drug manipulation. Changes shown are mean differences from pre-infusion values. Error bars denote S.E.M.. Single, double and triple asterisks denote significance at p<0.05, p<0.01, and p<0.001, respectively.

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