Frontal Feedback-Related Potentials in Nonhuman Primates: Modulation during Learning and under Haloperidol

Abstract

Feedback monitoring and adaptation of performance involve a medial reward system including medial frontal cortical areas, the medial striatum, and the dopaminergic system. A considerable amount of data has been obtained on frontal surface feedback-related potentials (FRPs) in humans and on the correlate of outcome monitoring with single unit activity in monkeys. However, work is needed to bridge knowledge obtained in the two species. The present work describes FRPs in monkeys, using chronic recordings, during a trial and error task. We show that frontal FRPs are differentially sensitive to successes and failures and can be observed over long-term periods. In addition, using the dopamine antagonist haloperidol we observe a selective effect on FRP amplitude that is absent for pure sensoryrelated potentials. These results describe frontal dopaminergic-dependent FRPs in monkeys and corroborate a human-monkey homology for performance monitoring signals.

Prefrontal Markers and Cognitive Performance Are Dissociated during Progressive Dopamine Lesion

“…Once monkeys had found the rewarded location, they could repeat that rewarded choice three times (repetition phase, REP), before a signal to change (STC) informed them that the rewarded location had been re-randomized. Previous research has shown that the PST induces high or low cognitive control on different trials [8,12,18,23]. Low control is sufficient on any repetition trial after correct feedback, as the monkey simply has to repeat the previous choice.…”

“…High control is required when the outcome of the previous trial necessitates a behavioural adaptation—notably, in three cases, after an incorrect feedback, after an STC directing a new SEA phase, and after the monkey makes a break in fixation or touch. This task is a well-established test of cognitive control with well-established neural correlates, notably delay activity in PFC comparable to working memory tasks [18] and feedback responses sensitive to dopamine [8]. As such, it allows us to probe control in terms of both performance monitoring and control implementation.…”

“…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) [5–7], 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]).…”

“…First, the mesocortical dopaminergic projections are thought to provide a prediction error signal that regulates performance monitoring functions implemented in MCC [10]. However, causal proof for this relation remains sparse [8], dopamine antagonist interventions have variable effects on behavioural outcomes [27,28], and so the functional significance of this link is debated [29]. Second, dopamine has been directly or indirectly linked to neurophysiological prefrontal mechanisms of cognitive control [30,31], working memory [32–34], and motivation [35].…”

Modulation of feedback related activity in the rostral anterior cingulate cortex during trial and error exploration

“…For this purpose, we adapted a problem-solving task developed for electrophysiological recording in monkeys (Quilodran et al, 2008;Rothe et al, 2011;Vezoli and Procyk, 2009). Subjects had to discover which one of the four presented stimuli was associated with correct feedback (i.e.…”