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Control of visual cortical signals by prefrontal dopamine.

Noudoost B, Moore T - Nature (2011)

Bottom Line: Experimental and clinical evidence indicate that prefrontal dopamine has an important role in cognitive functions, acting predominantly through D1 receptors.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.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.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute and Department of Neurobiology, Stanford University School of Medicine, Fairchild building, 299 Campus Drive West, Stanford, California 94305, USA. behrad@stanford.edu

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.

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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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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.

Mentions: The effect of the D1R manipulation on saccadic target selection was highly consistent across the two monkeys tested. Of 21 double-target experiments, the PES was reduced in every case (Fig. 3A). The mean PES shifted in favor of the FEFRF stimulus by an average of 27 ms (ΔPES=−26.934±3.086, p<10−3), significantly increasing the overall proportion of FEFRF choices (Chi-square=80.60, p<10−3), thus indicating that the D1R manipulation increased the monkeys’ tendency to target FEFRF stimuli. The increase in target selection was apparent across a range of drug dosages (Supplementary Fig. 5). In addition to the D1R manipulation, we tested the effects of the D2R-agonist quinpirole. Previous studies using this drug found that it does not affect persistent activity, but rather increases saccade-related activity within dorsolateral PFC20. We found that, like the D1R effect, local manipulation of D2R-mediated FEF activity increased the selection of FEFRF targets (Fig. 3A). The PES shifted an average of 22 ms (ΔPES=−21.993±6.758, p=0.010), increasing the proportion of FEFRF choices (Chi-square= 13.86, p<10−3). Thus, the D1R and D2R-mediated manipulations of FEF activity resulted in equivalent increases in saccadic target selection.


Control of visual cortical signals by prefrontal dopamine.

Noudoost B, Moore T - Nature (2011)

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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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3117113&req=5

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.
Mentions: The effect of the D1R manipulation on saccadic target selection was highly consistent across the two monkeys tested. Of 21 double-target experiments, the PES was reduced in every case (Fig. 3A). The mean PES shifted in favor of the FEFRF stimulus by an average of 27 ms (ΔPES=−26.934±3.086, p<10−3), significantly increasing the overall proportion of FEFRF choices (Chi-square=80.60, p<10−3), thus indicating that the D1R manipulation increased the monkeys’ tendency to target FEFRF stimuli. The increase in target selection was apparent across a range of drug dosages (Supplementary Fig. 5). In addition to the D1R manipulation, we tested the effects of the D2R-agonist quinpirole. Previous studies using this drug found that it does not affect persistent activity, but rather increases saccade-related activity within dorsolateral PFC20. We found that, like the D1R effect, local manipulation of D2R-mediated FEF activity increased the selection of FEFRF targets (Fig. 3A). The PES shifted an average of 22 ms (ΔPES=−21.993±6.758, p=0.010), increasing the proportion of FEFRF choices (Chi-square= 13.86, p<10−3). Thus, the D1R and D2R-mediated manipulations of FEF activity resulted in equivalent increases in saccadic target selection.

Bottom Line: Experimental and clinical evidence indicate that prefrontal dopamine has an important role in cognitive functions, acting predominantly through D1 receptors.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.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.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute and Department of Neurobiology, Stanford University School of Medicine, Fairchild building, 299 Campus Drive West, Stanford, California 94305, USA. behrad@stanford.edu

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.

Show MeSH
Related in: MedlinePlus