Abstract
Dopamine is thought to directly influence the neurophysiological mechanisms of both performance monitoring and cognitive control—two processes that are critically linked in the production of adapted behaviour. Changing dopamine levels are also thought to induce cognitive changes in several neurological and psychiatric conditions. But the working model of this system as a whole remains untested. Specifically, although many researchers assume that changing dopamine levels modify neurophysiological mechanisms and their markers in frontal cortex, and that this in turn leads to cognitive changes, this causal chain needs to be verified. Using longitudinal recordings of frontal neurophysiological markers over many months during progressive dopaminergic lesion in non-human primates, we provide data that fail to support a simple interaction between dopamine, frontal function, and cognition. Feedback potentials, which are performance-monitoring signals sometimes thought to drive successful control, ceased to differentiate feedback valence at the end of the lesion, just before clinical motor threshold. In contrast, cognitive control performance and beta oscillatory markers of cognitive control were unimpaired by the lesion. The differing dynamics of these measures throughout a dopamine lesion suggests they are not all driven by dopamine in the same way. These dynamics also demonstrate that a complex non-linear set of mechanisms is engaged in the brain in response to a progressive dopamine lesion. These results question the direct causal chain from dopamine to frontal physiology and on to cognition. They imply that biomarkers of cognitive functions are not directly predictive of dopamine loss.
Highlights
Successful and adaptive completion of cognitive tasks requires tight integration between performance monitoring [1,2], which provides information about task outcomes, and cognitive control [3], which drives behavioural adaptation as necessary
It has been suggested that cognitive control, performance monitoring, and their neurophysiological markers are under the influence of dopamine
The oscillatory signals showed only subtle changes in comparison, despite the depletion. Together these results bring into question the simple idea that dopamine directly modulates frontal cortex, which in turn directly modulates cognition
Summary
Successful and adaptive completion of cognitive tasks requires tight integration between performance monitoring [1,2], which provides information about task outcomes, and cognitive control [3], which drives behavioural adaptation as necessary These systems are associated with neurophysiological markers in the frontal lobes that are modulated by motivation [4]. Error- and feedback-related potentials (error-related negativity [ERN] and feedback potentials [FRPs]) recorded over the medial part of the frontal lobe in electroencephalography (EEG) [5,6,7], electrocorticography (ECoG) [8], and local field potential (LFP) [9] differentiate outcome valences These performance-monitoring signals are in many cases generated in midcingulate cortex (MCC [10,11]). Beta oscillations are implicated in top-down control of behaviour in cognitively engaging tasks [19,20,21,22], whilst altering within-session to reflect attentional effort on the task [23]
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