Alexandre Zénon

Superior Colliculus and Visual Spatial Attention

The superior colliculus (SC) has long been known to be part of the network of brain areas involved in spatial attention, but recent findings have dramatically refined our understanding of its functional role. The SC both implements the motor consequences of attention and plays a crucial role in the process of target selection that precedes movement. Moreover, even in the absence of overt orienting movements, SC activity is related to shifts of covert attention and is necessary for the normal control of spatial attention during perceptual judgments. The neuronal circuits that link the SC to spatial attention may include attention-related areas of the cerebral cortex, but recent results show that the SCs contribution involves mechanisms that operate independently of the established signatures of attention in visual cortex. These findings raise new issues and suggest novel possibilities for understanding the brain mechanisms that enable spatial attention.

Attention deficits without cortical neuronal deficits

The ability to process relevant stimuli selectively is a fundamental function of the primate visual system. The best-understood correlate of this function is the enhanced response of neurons in the visual cortex to attended stimuli. However, recent results show that the superior colliculus (SC), a midbrain structure, also has a crucial role in visual attention. It has been assumed that the SC acts through the same well-known mechanisms in the visual cortex. Here we tested this hypothesis by transiently inactivating the SC during a motion-change-detection task and measuring responses in two visual cortical areas. We found that despite large deficits in visual attention, the enhanced responses of neurons in the visual cortex to attended stimuli were unchanged. These results show that the SC contributes to visual attention through mechanisms that are independent of the classic effects in the visual cortex, demonstrating that other processes must have key roles in visual attention.

Salience representation in the parietal and frontal cortex

Some objects in the visual field are more likely to attract attention because they are either intrinsically eye catching or relevant in the context of a particular task. These two factors, known as stimulus-driven and goal-directed factors, respectively, are thought to be integrated into a unique salience map, possibly located in the frontal or the parietal cortex. However, the distinct contribution of these two regions to salience representation is difficult to establish experimentally and remains debated. In an attempt to address this issue, we designed several dual tasks composed of a letter reporting task and a visual search task, allowing us to quantify the salience of each visual item by measuring its probability to be selected by attention. In Experiment 1, the salience of the visual search items depended on a combination of conspicuity and relevance factors, whereas in Experiment 2, stimulus-driven and goal-directed factors were tested separately. Then, we used transcranial magnetic stimulation to interfere transiently with the function of the right angular gyrus (ANG) or right FEFs in healthy subjects performing these dual tasks. We found that interfering with the ANG and the FEF function specifically altered the influence of salience on the letter report rate without affecting the overall letter reporting rate, suggesting that these areas are involved in salience representation. In particular, the present study suggests that ANG is involved in goal-directed salience representation, whereas FEF would rather house a global salience map integrating both goal-directed and stimulus-driven factors.

Dissociation between mental fatigue and motivational state during prolonged mental activity

Mental fatigue (MF) is commonly observed following prolonged cognitive activity and can have major repercussions on the daily life of patients as well as healthy individuals. Despite its important impact, the cognitive processes involved in MF remain largely unknown. An influential hypothesis states that MF does not arise from a disruption of overused neural processes but, rather, is caused by a progressive decrease in motivation-related task engagement. Here, to test this hypothesis, we measured various neural, autonomic, psychometric and behavioral signatures of MF and motivation (EEG, ECG, pupil size, eye blinks, Skin conductance responses (SCRs), questionnaires and performance in a working memory (WM) task) in healthy volunteers, while MF was induced by Sudoku tasks performed for 120 min. Moreover extrinsic motivation was manipulated by using different levels of monetary reward. We found that, during the course of the experiment, the participants’ subjective feeling of fatigue increased and their performance worsened while their blink rate and heart rate variability (HRV) increased. Conversely, reward-induced EEG, pupillometric and skin conductance signal changes, regarded as indicators of task engagement, remained constant during the experiment, and failed to correlate with the indices of MF. In addition, MF did not affect a simple reaction time task, despite the strong influence of extrinsic motivation on this task. Finally, alterations of the motivational state through monetary incentives failed to compensate the effects of MF. These findings indicate that MF in healthy subjects is not caused by an alteration of task engagement but is likely to be the consequence of a decrease in the efficiency, or availability, of cognitive resources.

The human subthalamic nucleus encodes the subjective value of reward and the cost of effort during decision-making

Adaptive behaviour entails the capacity to select actions as a function of their energy cost and expected value and the disruption of this faculty is now viewed as a possible cause of the symptoms of Parkinsons disease. Indirect evidence points to the involvement of the subthalamic nucleus-the most common target for deep brain stimulation in Parkinsons disease-in cost-benefit computation. However, this putative function appears at odds with the current view that the subthalamic nucleus is important for adjusting behaviour to conflict. Here we tested these contrasting hypotheses by recording the neuronal activity of the subthalamic nucleus of patients with Parkinsons disease during an effort-based decision task. Local field potentials were recorded from the subthalamic nucleus of 12 patients with advanced Parkinsons disease (mean age 63.8 years ± 6.8; mean disease duration 9.4 years ± 2.5) both OFF and ON levodopa while they had to decide whether to engage in an effort task based on the level of effort required and the value of the reward promised in return. The data were analysed using generalized linear mixed models and cluster-based permutation methods. Behaviourally, the probability of trial acceptance increased with the reward value and decreased with the required effort level. Dopamine replacement therapy increased the rate of acceptance for efforts associated with low rewards. When recording the subthalamic nucleus activity, we found a clear neural response to both reward and effort cues in the 1-10 Hz range. In addition these responses were informative of the subjective value of reward and level of effort rather than their actual quantities, such that they were predictive of the participants decisions. OFF levodopa, this link with acceptance was weakened. Finally, we found that these responses did not index conflict, as they did not vary as a function of the distance from indifference in the acceptance decision. These findings show that low-frequency neuronal activity in the subthalamic nucleus may encode the information required to make cost-benefit comparisons, rather than signal conflict. The link between these neural responses and behaviour was stronger under dopamine replacement therapy. Our findings are consistent with the view that Parkinsons disease symptoms may be caused by a disruption of the processes involved in balancing the value of actions with their associated effort cost.

Dissociable contribution of the parietal and frontal cortex to coding movement direction and amplitude

To reach for an object, we must convert its spatial location into an appropriate motor command, merging movement direction and amplitude. In humans, it has been suggested that this visuo-motor transformation occurs in a dorsomedial parieto-frontal pathway, although the causal contribution of the areas constituting the “reaching circuit” remains unknown. Here we used transcranial magnetic stimulation (TMS) in healthy volunteers to disrupt the function of either the medial intraparietal area (mIPS) or dorsal premotor cortex (PMd), in each hemisphere. The task consisted in performing step-tracking movements with the right wrist towards targets located in different directions and eccentricities; targets were either visible for the whole trial (Target-ON) or flashed for 200 ms (Target-OFF). Left and right mIPS disruption led to errors in the initial direction of movements performed towards contralateral targets. These errors were corrected online in the Target-ON condition but when the target was flashed for 200 ms, mIPS TMS manifested as a larger endpoint spreading. In contrast, left PMd virtual lesions led to higher acceleration and velocity peaks—two parameters typically used to probe the planned movement amplitude—irrespective of the target position, hemifield and presentation condition; in the Target-OFF condition, left PMd TMS induced overshooting and increased the endpoint dispersion along the axis of the target direction. These results indicate that left PMd intervenes in coding amplitude during movement preparation. The critical TMS timings leading to errors in direction and amplitude were different, namely 160–100 ms before movement onset for mIPS and 100–40 ms for left PMd. TMS applied over right PMd had no significant effect. These results demonstrate that, during motor preparation, direction and amplitude of goal-directed movements are processed by different cortical areas, at distinct timings, and according to a specific hemispheric organization.

Similar effect of cueing conditions on attentional and saccadic temporal dynamics

Spatial attention permits to allocate more processing resources to a restricted portion of the visual space. The influential premotor theory states that the allocation of spatial attention relies on the same processes as those responsible for programming saccadic eye movements. Accordingly, several studies have already demonstrated a close spatial correspondence between attention and saccades. However, the question of the temporal coupling between attention displacements and saccades remains unclear. To address this issue, we compared the saccadic latencies to the temporal dynamics of attentional shifts under various cueing conditions known to affect attentional timing. In Experiment 1, we evaluated the effect of peripheral and central cues, and in Experiment 2, we assessed the influence of peripheral cues of different salience levels. We found that the different cue types had a similar effect on saccade latencies and on the dynamics of attentional shifts, either overt or covert. Moreover, even within a given cueing condition, attentional shift times were strongly correlated with saccadic latencies. These results indicate that, in agreement with the premotor theory, both spatial attention and saccades rely on a common process and that the allocation of spatial attention is tightly time-locked to saccade execution.

Dopamine Manipulation Affects Response Vigor Independently of Opportunity Cost.

Dopamine is known to be involved in regulating effort investment in relation to reward, and the disruption of this mechanism is thought to be central in some pathological situations such as Parkinsons disease, addiction, and depression. According to an influential model, dopamine plays this role by encoding the opportunity cost, i.e., the average value of forfeited actions, which is an important parameter to take into account when making decisions about which action to undertake and how fast to execute it. We tested this hypothesis by asking healthy human participants to perform two effort-based decision-making tasks, following either placebo or levodopa intake in a double blind within-subject protocol. In the effort-constrained task, there was a trade-off between the amount of force exerted and the time spent in executing the task, such that investing more effort decreased the opportunity cost. In the time-constrained task, the effort duration was constant, but exerting more force allowed the subject to earn more substantial reward instead of saving time. Contrary to the model predictions, we found that levodopa caused an increase in the force exerted only in the time-constrained task, in which there was no trade-off between effort and opportunity cost. In addition, a computational model showed that dopamine manipulation left the opportunity cost factor unaffected but altered the ratio between the effort cost and reinforcement value. These findings suggest that dopamine does not represent the opportunity cost but rather modulates how much effort a given reward is worth. SIGNIFICANCE STATEMENT Dopamine has been proposed in a prevalent theory to signal the average reward rate, used to estimate the cost of investing time in an action, also referred to as opportunity cost. We contrasted the effect of dopamine manipulation in healthy participants in two tasks, in which increasing response vigor (i.e., the amount of effort invested in an action) allowed either to save time or to earn more reward. We found that levodopa—a synthetic precursor of dopamine—increases response vigor only in the latter situation, demonstrating that, rather than the opportunity cost, dopamine is involved in computing the expected value of effort.

Spatial and temporal dynamics of attentional guidance during inefficient visual search

Spotting a prey or a predator is crucial in the natural environment and relies on the ability to extract quickly pertinent visual information. The experimental counterpart of this behavior is visual search (VS) where subjects have to identify a target amongst several distractors. In difficult VS tasks, it has been found that the reaction time (RT) is influenced by salience factors, such as the target-distractor similarity, and this finding is usually regarded as evidence for a guidance of attention by preattentive mechanisms. However, the use of RT measurements, a parameter which depends on multiple factors, allows only very indirect inferences about the underlying attentional mechanisms. The purpose of the present study was to determine the influence of salience factors on attentional guidance during VS, by measuring directly attentional allocation. We studied attention allocation by using a dual covert VS task in subjects who had 1) to detect a target amongst different items and 2) to report letters briefly flashed inside those items at different delays. As predicted, we showed that parallel processes guide attention towards the most relevant item by virtue of both goal-directed and stimulus-driven factors, and we demonstrated that this attentional selection is a prerequisite for target detection. In addition, we show that when the target is characterized by two features (conjunction VS), the goal-directed effects of both features are initially combined into a unique salience value, but at a later stage, grouping phenomena interact with the salience computation, and lead to the selection of a whole group of items. These results, in line with Guided Search Theory, show that efficient and rapid preattentive processes guide attention towards the most salient item, allowing to reduce the number of attentional shifts needed to find the target.

Attentional guidance relies on a winner-take-all mechanism

The finding that attention can encompass several non-contiguous items at once challenges the current models of visual search based on a winner-take-all mechanism assuming the selection of a single object. It has been proposed instead that attentional guidance involves mechanisms selecting all relevant items simultaneously. In order to test this hypothesis, we studied attentional allocation during various visual search tasks. We confirmed that attention can indeed select several items concurrently but on the basis of their spatial relation, not relevance. This finding corroborates the view that during visual search, attentional guidance is based on a winner-take-all mechanism.