Dopamine Activation Preserves Visual Motion Perception Despite Noise Interference of Human V5/MT

Abstract

When processing sensory signals, the brain must account for noise, both noise in the stimulus and that arising from within its own neuronal circuitry. Dopamine receptor activation is known to enhance both visual cortical signal-to-noise-ratio (SNR) and visual perceptual performance; however, it is unknown whether these two dopamine-mediated phenomena are linked. To assess this, we used single-pulse transcranial magnetic stimulation (TMS) applied to visual cortical area V5/MT to reduce the SNR focally and thus disrupt visual motion discrimination performance to visual targets located in the same retinotopic space. The hypothesis that dopamine receptor activation enhances perceptual performance by improving cortical SNR predicts that dopamine activation should antagonize TMS disruption of visual perception. We assessed this hypothesis via a double-blinded, placebo-controlled study with the dopamine receptor agonists cabergoline (a D2 agonist) and pergolide (a D1/D2 agonist) administered in separate sessions (separated by 2 weeks) in 12 healthy volunteers in a William's balance-order design. TMS degraded visual motion perception when the evoked phosphene and the visual stimulus overlapped in time and space in the placebo and cabergoline conditions, but not in the pergolide condition. This suggests that dopamine D1 or combined D1 and D2 receptor activation enhances cortical SNR to boost perceptual performance. That local visual cortical excitability was unchanged across drug conditions suggests the involvement of long-range intracortical interactions in this D1 effect. Because increased internal noise (and thus lower SNR) can impair visual perceptual learning, improving visual cortical SNR via D1/D2 agonist therapy may be useful in boosting rehabilitation programs involving visual perceptual training.

Conscious perception and the modulatory role of dopamine: no effect of the dopamine D2 agonist cabergoline on visual masking, the attentional blink, and probabilistic discrimination

“…Yet, our Bayesian results without exception provided evidence against an effect of 1.5mg cabergoline (all BF incl < .7). This absence of an effect is further strengthened by the fact that other studies using different cognitive tasks have previously reported significant effects of cabergoline on task performance using a similar or an even lower dose of orally administered cabergoline (Broadway, Frank, & Cavanagh, 2018;Cavanagh et al, 2014;Fallon, Zokaei, Norbury, Manohar, & Husain, 2017;Frank & O'Reilly, 2006;Nandam et al, 2013;Yousif et al, 2016). These observations together argue for an interpretation in terms of a true null result.…”

The system‐neurophysiological basis for how methylphenidate modulates perceptual–attentional conflicts during auditory processing

“…Several lines of evidence suggest that the dopaminergic system, which MPH also targets, regulates the SNR of neural information processing; that is, it affects gain modulation principles (Li et al, 2001;Servan-Schreiber et al, 1990;Yousif et al, 2016;Ziegler et al, 2016). …”

“…Both the dopamine system (Li et al, 2001;Servan-Schreiber et al, 1990;Yousif et al, 2016;Ziegler et al, 2016) underlying the resolution of perceptual-attentional conflicts.…”

“…Several lines of evidence suggest that the DA system not only affects top-down attentional control processes (Noudoost & Moore, 2011b;Sarter, Albin, Kucinski, & Lustig, 2014;Sarter, Gehring, & Kozak, 2006) (Colzato, Pratt, & Hommel, 2010;Colzato, Slagter, de Rover, & Hommel, 2011), but also modulates bottom-up perceptual processes (Bao, Chan, & Merzenich, 2001;Noudoost & Moore, 2011a;Ziegler, Pedersen, Mowinckel, & Biele, 2016), possibly by improving the signal-to-noise ratio (SNR) of sensory input (Kroener, Chandler, Phillips, & Seamans, 2009;Yousif et al, 2016). This modulation of the SNR is considered to reflect neuronal gain control mechanisms (Li, Lindenberger, & Sikström, 2001;Servan-Schreiber, Printz, & Cohen, 1990;Yousif et al, 2016;Ziegler et al, 2016). Increasing gain control can be conceptualized as amplifying an information processing system's responsivity to input signals from multiple levels, for example, from the sensory level (Salinas & Thier, 2000).…”

“…Notably, the C-cluster is also crucial to consider regarding MPH effects of perceptual-attentional conflicts: The reason is that stimulus-response translation processes reflected by the C-cluster have been shown to be modulated during conflict resolution processes (Bluschke, Chmielewski, Mückschel, Roessner, & Beste, 2017;Schreiter et al, 2018). Furthermore, the dopamine system (Li et al, 2001;Li & Sikström, 2002;Servan-Schreiber et al, 1990;Yousif et al, 2016;Ziegler et al, 2016) as well as the norepinephrine system Mückschel, Chmielewski et al, 2017) have been shown to affect task context representation, task-related decision, or response selection processes during the resolution of processing conflicts. Moreover, modulations of the C-cluster are associated with the inferior parietal cortex (temporoparietal junction, TPJ, BA40) and the superior parietal cortex (BA7) (Bodmer & Beste, 2017;Wolff et al, 2017).…”