Sanjay Manohar

Reward Pays the Cost of Noise Reduction in Motor and Cognitive Control.

Summary Speed-accuracy trade-off is an intensively studied law governing almost all behavioral tasks across species. Here we show that motivation by reward breaks this law, by simultaneously invigorating movement and improving response precision. We devised a model to explain this paradoxical effect of reward by considering a new factor: the cost of control. Exerting control to improve response precision might itself come at a cost—a cost to attenuate a proportion of intrinsic neural noise. Applying a noise-reduction cost to optimal motor control predicted that reward can increase both velocity and accuracy. Similarly, application to decision-making predicted that reward reduces reaction times and errors in cognitive control. We used a novel saccadic distraction task to quantify the speed and accuracy of both movements and decisions under varying reward. Both faster speeds and smaller errors were observed with higher incentives, with the results best fitted by a model including a precision cost. Recent theories consider dopamine to be a key neuromodulator in mediating motivational effects of reward. We therefore examined how Parkinson’s disease (PD), a condition associated with dopamine depletion, alters the effects of reward. Individuals with PD showed reduced reward sensitivity in their speed and accuracy, consistent in our model with higher noise-control costs. Including a cost of control over noise explains how reward may allow apparent performance limits to be surpassed. On this view, the pattern of reduced reward sensitivity in PD patients can specifically be accounted for by a higher cost for controlling noise.

Individual Differences in Premotor Brain Systems Underlie Behavioral Apathy

Lack of physical engagement, productivity, and initiative—so-called “behavioral apathy”—is a common problem with significant impact, both personal and economic. Here, we investigate whether there might be a biological basis to such lack of motivation using a new effort and reward-based decision-making paradigm, combined with functional and diffusion-weighted imaging. We hypothesized that behavioral apathy in otherwise healthy people might be associated with differences in brain systems underlying either motivation to act (specifically in effort and reward-based decision-making) or in action processing (transformation of an intention into action). The results demonstrate that behavioral apathy is associated with increased effort sensitivity as well as greater recruitment of neural systems involved in action anticipation: supplementary motor area (SMA) and cingulate motor zones. In addition, decreased structural and functional connectivity between anterior cingulate cortex (ACC) and SMA were associated with increased behavioral apathy. These findings reveal that effort sensitivity and translation of intentions into actions might make a critical contribution to behavioral apathy. We propose a mechanism whereby inefficient communication between ACC and SMA might lead to increased physiological cost—and greater effort sensitivity—for action initiation in more apathetic people.

Characterization of reward and effort mechanisms in apathy

Highlights • Apathy in the normal population is dissociable from depression and anhedonia.• Apathy in the normal population is related to the modulation of physical effort people are willing to engage.• Apathy in the normal population is associated with higher subjective effort costs for small rewards.

Contrast affects the strength of synesthetic colors

Grapheme-color synesthesia is an automatic, involuntary experience of seeing colors when viewing numbers, letters or words on a printed page. Previous research has demonstrated that synesthesia is a genuine perceptual phenomenon, but crucially, all of these experiments have used high-contrast letters and numbers. Our synesthete, JC, anecdotally reported that the strength of his synesthetic colors varied depending on whether the graphemes were presented in high or low contrast. To test this, we asked JC to rate the strength of his experiences to letters of different contrasts on three different dates. JCs ratings of the strength of his synesthetic colors consistently declined monotonically with contrast, suggesting that his synesthetic colors were reduced or absent at low contrasts. To more precisely quantify the impact of this, we then tested JC on modified versions of our embedded figures task (Ramachandran and Hubbard, 2001a) and crowding task (Ramachandran and Hubbard, 2001b) by presenting displays with varying contrast between the graphemes and the background. Behavioral data in the contrast variant of our embedded figures task showed that JC performed significantly better than controls at high contrast, replicating our previous findings. However, at low contrast this advantage was eliminated, consistent with his reports of weaker or absent colors. A similar, but weaker pattern of results was found in the modified version of our crowding task. These results suggest that JCs synesthetic colors may be elicited at contrast dependent stages of visual processing. We propose that regions of the fusiform gyrus specialized for letter and number grapheme recognition that have been shown to respond in a contrast dependent manner mediate JCs synesthetic colors. However, whether this is true for all grapheme-color synesthetes or is only true of the group we refer to as lower synesthetes, remains to be seen.

Causal Evidence for a Privileged Working Memory State in Early Visual Cortex

Emerging evidence suggests that items held in working memory (WM) might not all be in the same representational state. One item might be privileged over others, making it more accessible and thereby recalled with greater precision. Here, using transcranial magnetic stimulation (TMS), we provide causal evidence in human participants that items in WM are differentially susceptible to disruptive TMS, depending on their state, determined either by task relevance or serial position. Across two experiments, we applied TMS to area MT+ during the WM retention of two motion directions. In Experiment 1, we used an “incidental cue” to bring one of the two targets into a privileged state. In Experiment 2, we presented the targets sequentially so that the last item was in a privileged state by virtue of recency. In both experiments, recall precision of motion direction was differentially affected by TMS, depending on the state of the memory target at the time of disruption. Privileged items were recalled with less precision, whereas nonprivileged items were recalled with higher precision. Thus, only the privileged item was susceptible to disruptive TMS over MT+. By contrast, precision of the nonprivileged item improved either directly because of facilitation by TMS or indirectly through reduced interference from the privileged item. Our results provide a unique line of evidence, as revealed by TMS over a posterior sensory brain region, for at least two different states of item representation in WM.

Flexibility of representational states in working memory.

The relationship between working memory (WM) and attention is a highly interdependent one, with evidence that attention determines the state in which items in WM are retained. Through focusing of attention, an item might be held in a more prioritized state, commonly termed as the focus of attention (FOA). The remaining items, although still retrievable, are considered to be in a different representational state. One means to bring an item into the FOA is to use retrospective cues (“retro-cues”) which direct attention to one of the objects retained in WM. Alternatively, an item can enter a privileged state once attention is directed towards it through bottom-up influences (e.g., recency effect) or by performing an action on one of the retained items (“incidental” cueing). In all these cases, the item in the FOA is recalled with better accuracy compared to the other items in WM. Far less is known about the nature of the other items in WM and whether they can be flexibly manipulated in and out of the FOA. We present data from three types of experiments as well as transcranial magnetic stimulation (TMS) to early visual cortex to manipulate the item inside FOA. Taken together, our results suggest that the context in which items are retained in WM matters. When an item remains behaviorally relevant, despite not being inside the FOA, re-focusing attention upon it can increase its recall precision. This suggests that a non-FOA item can be held in a state in which it can be later retrieved. However, if an item is rendered behaviorally unimportant because it is very unlikely to be probed, it cannot be brought back into the FOA, nor recalled with high precision. Under such conditions, some information appears to be irretrievably lost from WM. These findings, obtained from several different methods, demonstrate quite considerable flexibility with which items in WM can be represented depending upon context. They have important consequences for emerging state-dependent models of WM.

The role of cognitive effort in subjective reward devaluation and risky decision-making

Motivation is underpinned by cost-benefit valuations where costs—such as physical effort or outcome risk—are subjectively weighed against available rewards. However, in many environments risks pertain not to the variance of outcomes, but to variance in the possible levels of effort required to obtain rewards (effort risks). Moreover, motivation is often guided by the extent to which cognitive—not physical—effort devalues rewards (effort discounting). Yet, very little is known about the mechanisms that underpin the influence of cognitive effort risks or discounting on motivation. We used two cost-benefit decision-making tasks to probe subjective sensitivity to cognitive effort (number of shifts of spatial attention) and to effort risks. Our results show that shifts of spatial attention when monitoring rapidly presented visual stimuli are perceived as effortful and devalue rewards. Additionally, most people are risk-averse, preferring safe, known amounts of effort over risky offers. However, there was no correlation between their effort and risk sensitivity. We show for the first time that people are averse to variance in the possible amount of cognitive effort to be exerted. These results suggest that cognitive effort sensitivity and risk sensitivity are underpinned by distinct psychological and neurobiological mechanisms.

Reward sensitivity deficits modulated by dopamine are associated with apathy in Parkinson’s disease

Apathy is extremely common in neurodegenerative disorders such as Parkinson’s disease. Muhammed et al. report that lack of sensitivity to rewards may underlie apathy, with dopamine playing a modulatory role. The study provides a basis for objective clinical markers of motivation and treatment efficacy in neurodegenerative conditions.

Past rewards capture spatial attention and action choices

AbstractThe desire to increase rewards and minimize punishing events is a powerful driver in behaviour. Here, we assess how the value of a location affects subsequent deployment of goal-directed attention as well as involuntary capture of attention on a trial-to-trial basis. By tracking eye position, we investigated whether the ability of an irrelevant, salient visual stimulus to capture gaze (stimulus-driven attention) is modulated by that location’s previous value. We found that distractors draw attention to them significantly more if they appear at a location previously associated with a reward, even when gazing towards them now leads to punishments. Within the same experiment, it was possible to demonstrate that a location associated with a reward can also bias subsequent goal-directed attention (indexed by action choices) towards it. Moreover, individuals who were vulnerable to being distracted by previous reward history, as indexed by oculomotor capture, were also more likely to direct their actions to those locations when they had a free choice. Even when the number of initial responses was made to be rewarded and punished stimuli were equalized, the effects of previous reward history on both distractibility and action choices remained. Finally, a covert attention task requiring button-press responses rather than overt gaze shifts demonstrated the same pattern of findings. Thus, past rewards can act to modulate both subsequent stimulus-driven as well as goal-directed attention. These findings reveal that there can be surprising short-term costs of using reward cues to regulate behaviour. They show that current valence information, if maintained inappropriately, can have negative subsequent effects, with attention and action choices being vulnerable to capture and bias, mechanisms that are of potential importance in understanding distractibility and abnormal action choices.

Human ventromedial prefrontal lesions alter incentivisation by reward.

Although medial frontal brain regions are implicated in valuation of rewards, evidence from focal lesions to these areas is scant, with many conflicting results regarding motivation and affect, and no human studies specifically examining incentivisation by reward. Here, 19 patients with isolated, focal damage in ventral and medial prefrontal cortex were selected from a database of 453 individuals with subarachnoid haemorrhage. Using a speeded saccadic task based on the oculomotor capture paradigm, we manipulated the maximum reward available on each trial using an auditory incentive cue. Modulation of behaviour by motivation permitted quantification of reward sensitivity. At the group level, medial frontal damage was overall associated with significantly reduced effects of reward on invigorating saccadic velocity and autonomic (pupil) responses compared to age-matched, healthy controls. Crucially, however, some individuals instead showed abnormally strong incentivisation effects for vigour. Increased sensitivity to rewards within the lesion group correlated with damage in subgenual ventromedial prefrontal cortex (vmPFC) areas, which have recently become the target for deep brain stimulation (DBS) in depression. Lesion correlations with clinical apathy suggested that the apathy associated with prefrontal damage is in fact reduced by damage at those coordinates. Reduced reward sensitivity showed a trend to correlate with damage near nucleus accumbens. Lesions did not, on the other hand, influence reward sensitivity of cognitive control, as measured by distractibility. Thus, although medial frontal lesions may generally reduce reward sensitivity, damage to key subregions paradoxically protect from this effect.