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Grogan, J. P.

Publications and source records attributed to Grogan, J. P..

8 recordsLinked to original sources

Neural dynamics of covert habit activation and control in humans

The neuroscience of habits in humans presumes a competition between two systems: stimulus-response and goal-directed. But lacking strong causal manipulations for inducing habits in humans, researchers have struggled to understand the brain mechanisms supporting the development of stimulus-response associations over time and their interaction with goal-directed processes. To address this, we conducted a preregistered electroencephalography (EEG) study with 14 days of stimulus-response training and used tight temporal controls to isolate the functioning of each system. In line with our preregistered hypothesis, we found that the lateralized readiness potential (LRP) tracked covert activation of habitual responses, detectable on trials where inappropriate habits are overcome and behavior is classed as goal-directed. In exploratory analyses, the strength of this covert habitual activation was associated with the degree of inappropriate habit expression on separate trials where response preparation time was limited. Further, exploratory analyses suggested that frontal midline theta (FM{theta}) power was selectively elevated when extensively trained habits needed to be overridden, and that this elevation scaled with individual differences in habit expression. These data provide evidence consistent with a dual systems account in which habit expression reflects competition between distinct neural subsystems and offer a new window into the formation and override of habits.

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Neurally-informed modelling unravels a single evidence accumulation process for choices and subsequent confidence reports

How is the content of our decision making processes translated into subjective confidence? Current computational models designed to account for choice- and confidence-reporting behaviour disagree on two fundamental questions: do choice and confidence reports arise from shared versus distinct evaluation processes and what stopping-rule is applied to evidence sampling for confidence reports? Here, we employed a neurally-informed modelling approach in which competing models were compared both based on their fits to behaviour and their ability to recapitulate human electrophysiological signatures of evidence accumulation. Participants made self-paced confidence reports after indicating perceptual choices on a random dot motion task. Model comparison based on behavioural data alone showed that boundary-based stopping rules for confidence reporting provided superior fits than time-based stopping rules. However, results were inconclusive when comparing models with a single evidence accumulation process dictating choice and confidence reports compared to models invoking distinct processes. Importantly, the single-process model markedly outperformed the other models in its ability to account for the observed neural evidence accumulation patterns, including the fact that signal amplitudes predicted reported confidence several hundred milliseconds before the initial choice had been reported. Our study demonstrates that choice behaviour, subjective confidence, and associated neural decision signals can be jointly explained by a model invoking a single process of evidence accumulation with separate boundaries for the initial choice and subsequent confidence reports. Significance StatementHow does the brain generate representations of subjective confidence from categorical decisions? While some models suggest that confidence arises from a read-out of the same information that determined the initial choice, others propose that confidence is determined by a distinct computational process. Definitively testing these alternative accounts has proven difficult because they often make similar predictions for behavioural data. Here, we employ a novel neurally-informed modelling method that evaluates models based on their ability to reproduce key neurophysiological signatures of choice and confidence in addition to behaviour. Our results indicate that choices and subjective confidence are determined by a shared sensory evidence accumulation process.

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Confidence is predicted by pre- and post-choice decision signal dynamics

It is well established that ones confidence in a choice can be influenced by new evidence encountered after commitment has been reached, but the processes through which post-choice evidence is sampled remain unclear. To investigate this, we traced the pre- and post-choice dynamics of electrophysiological signatures of evidence accumulation (Centro-parietal Positivity, CPP) and motor preparation (mu/beta band) to determine their sensitivity to participants confidence in their perceptual discriminations. Pre-choice CPP amplitudes scaled with confidence both when confidence was reported simultaneously with choice, or when reported 1-second after the initial direction decision. When additional evidence was presented during the post-choice delay period, the CPP continued to evolve after the initial choice, with a more prolonged build-up on trials with lower confidence in the alternative that was finally endorsed, irrespective of whether this entailed a change-of-mind. Further investigation established that this pattern was accompanied by earlier post-choice CPP peak latency, earlier lateralisation of motor preparation signals toward the ultimately chosen response, and faster confidence reports when participants indicated high certainty that they had made a correct or incorrect initial choice. These observations are consistent with confidence-dependent stopping theories according to which post-choice evidence accumulation ceases when a criterion level of confidence in a choice alternative has been reached. Our findings have implications for current models of choice confidence, and predictions they may make about EEG signatures.

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Muscarinic receptors mediate motivation via preparatory neural activity in humans

Motivation depends on dopamine, but might be modulated by acetylcholine which influences dopamine release in the striatum, and amplifies motivation in animal studies. A corresponding effect in humans would be important clinically, since anticholinergic drugs are frequently used in Parkinsons disease, a condition that can also disrupt motivation. Reward and dopamine make us more ready to respond, as indexed by reaction times (RT), and move faster, sometimes termed vigour. These effects may be controlled by preparatory processes that can be tracked using electroencephalography (EEG). We measured vigour in a placebo-controlled, double-blinded study of trihexyphenidyl (THP), a muscarinic antagonist, with an incentivised eye movement task and EEG. Participants responded faster and with greater vigour when incentives were high, but THP blunted these motivation effects, suggesting that muscarinic receptors facilitate invigoration by reward. Preparatory EEG build-up (contingent negative variation; CNV) was strengthened by high incentives and by muscarinic blockade, although THP reduced the incentive-effect. The amplitude of preparatory activity predicted both vigour and RT, although over distinct scalp regions; frontal activity predicted vigour, whereas a larger, earlier, central component predicted RT. The incentivisation of RT was partly mediated by the CNV, though vigour was not. Moreover, the CNV mediated the drugs effect on dampening incentives, suggesting that muscarinic receptors underlie the motivational influence on this preparatory activity. Taken together, these findings show that a muscarinic blocker impairs motivated action in healthy people, and that medial frontal preparatory neural activity mediates this for RT.

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Dopamine-gated memory selection during slow wave sleep

The human brain selectively stores knowledge of the world to optimise future behaviour, automatically rehearsing, contextualising or discarding information to create a robust record of experiences. Storage or forgetting evolves over time, particularly during sleep. We have previously shown that dopamine given in the form of L-DOPA tablets improves long-term memory in Parkinsons disease, but only when given overnight. L-DOPA is already prescribed widely with a good safety profile and could potentially be rapidly repurposed to improve cognitive performance and improve quality of life in, for example, early Alzheimers Disease, if we understood the best time of day to prescribe. Therefore, we sought to test how dopamine shaped long-term memory formation before and during sleep in a double-blind randomised placebo-controlled cross-over trial of healthy older adults (n = 35). We administered L-DOPA after word-list learning to be active during repeat exposure to a proportion of the words and during subsequent nocturnal sleep. Nocturnal dopamine accelerated forgetting for words presented once but it did not affect memory for words presented twice. During slow wave sleep, L-DOPA also increased spindle amplitude around slow oscillation peaks. Larger dopamine-induced difference in word memory was associated with a larger increase in spindle amplitude. Dopamine-dependent memory processing may therefore modulate spindles dependent on slow-oscillation phase. Further, overnight dopamine increased total slow wave sleep duration by approximately 11%. This pharmaceutical modification of slow wave sleep may have potential health-enhancing benefits in old age that could include cognitive enhancement and Alzheimers prevention. One Sentence SummaryDopamine before sleep promotes forgetting of weak memory traces associated with increased spindle amplitude around the peak of a slow oscillations.

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Dopamine promotes instrumental motivation, but reduces reward-related vigour

We can be motivated when reward depends on performance, or merely by the prospect of a guaranteed reward. Performance-dependent (contingent) reward is instrumental, relying on an internal action-outcome model, whereas motivation by guaranteed reward may serve to minimise opportunity cost in reward-rich environments. Competing theories propose that each type of motivation should be dependent on dopaminergic activity. We contrasted these two types of motivation with a rewarded saccade task, in patients with Parkinsons disease (PD). When PD patients were ON dopamine, they had greater response vigour (peak saccadic velocity) for contingent rewards, whereas when PD patients were OFF medication, they had greater vigour for guaranteed rewards. These results support the view that reward expectation and contingency drive distinct motivational processes, and can be dissociated by manipulating dopaminergic activity. We posit that dopamine is necessary for goal-directed motivation, but dampens reward-driven vigour, challenging the theory that tonic dopamine encodes reward expectation.

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Levodopa’s effects on expression of reinforcement learning

Dopamine has been implicated in learning from rewards and punishment, and in the expression of this learning. However, many studies do not fully separate retrieval and decision mechanisms from learning and consolidation. Here, we investigated the effects of levodopa (dopamine precursor) on choice performance (isolated from learning or consolidation). We gave 31 healthy older adults 150mg of levodopa or placebo (double-blinded, randomised) 1 hour before testing them on stimuli they had learned the value of the previous day. We found that levodopa did not affect the overall accuracy of choices, nor the relative expression of positively or negatively reinforced values. This contradicts several studies and suggests that dopamine may not play a role in the choice performance for values learned through reinforcement learning in humans.

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Effects of Parkinson’s disease and dopamine on digit span measures of working memory

RationaleParkinsons disease (PD) impairs working memory (WM) - the ability to maintain items in memory for short periods of time and manipulate them. There is conflicting evidence on the nature of the deficits caused by the disease, and the potential beneficial and detrimental effects of dopaminergic medication on different WM processes.\n\nObjectivesWe hypothesised that PD impairs both maintenance and manipulation of items in WM and dopaminergic medications improve this in PD patients but impair it in healthy older adults.\n\nMethodsWe tested 68 PD patients ON and OFF their dopaminergic medication, 83 healthy age-matched controls, and 30 healthy older adults after placebo and levodopa administration. We used the digit span, a WM test with three components (forwards, backwards and sequence recall) that differ in the amount of manipulation required. We analysed the maximum spans and the percentage of lists correctly recalled, which probe capacity of WM and the accuracy of the memory processes within this capacity, respectively.\n\nResultsPD patients had lower WM capacity across all three digit span components, but only showed reduced percentage accuracy on the components requiring manipulation (backwards and sequence spans). Dopaminergic medication did not affect performance in PD patients. In healthy older adults, levodopa did not affect capacity, but did impair accuracy on one of the manipulation components (sequence), without affecting the other (backwards).\n\nConclusionsThis suggests a non-dopaminergic deficit of maintenance capacity and manipulation accuracy in PD patients, and a potential \"overdosing\" of intact manipulation mechanisms in healthy older adults by levodopa.

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