Marcus Missal

Tagging the Neuronal Entrainment to Beat and Meter

Feeling the beat and meter is fundamental to the experience of music. However, how these periodicities are represented in the brain remains largely unknown. Here, we test whether this function emerges from the entrainment of neurons resonating to the beat and meter. We recorded the electroencephalogram while participants listened to a musical beat and imagined a binary or a ternary meter on this beat (i.e., a march or a waltz). We found that the beat elicits a sustained periodic EEG response tuned to the beat frequency. Most importantly, we found that meter imagery elicits an additional frequency tuned to the corresponding metric interpretation of this beat. These results provide compelling evidence that neural entrainment to beat and meter can be captured directly in the electroencephalogram. More generally, our results suggest that music constitutes a unique context to explore entrainment phenomena in dynamic cognitive processing at the level of neural networks.

Divergence between oculomotor and perceptual causality

When two objects such as billiard balls collide, observers perceive that the action of one caused the motion of the other. We have previously shown (Badler, Lefèvre, & Missal, 2010) that this extends to the oculomotor domain: subjects make more predictive movements in the expected direction of causal motion than in a noncausal direction. However, predictive oculomotor and reactive psychophysical responses have never been directly compared. They should be correlated if they tap into the same mental processes. To test this, we recorded oculomotor responses to launching stimuli, then asked subjects to manually classify those stimuli as causal or noncausal. Overall the psychophysical classifications matched the oculomotor biases, although correlations across subjects were mostly absent. In subsequent experiments, 50% of the trials had a 300-millisecond delay after the collision to impede the perception of causality. Subjects maintained their causal oculomotor bias but used different classification strategies, usually grouping the stimuli either by delay or by direction. In addition, there was no evidence that the two response types were correlated on a trial-by-trial basis. The results suggest divergent processes underlying oculomotor responses to and judgments of causal stimuli.

A dynamic representation of target motion drives predictive smooth pursuit during target blanking.

Moving objects are often occluded by neighboring objects. In order for the eye to smoothly pursue a moving object that is transiently occluded, a prediction of its trajectory is necessary. For targets moving on a linear path, predictive eye velocity can be regulated on the basis of target motion before and after the occlusions. However, objects in a more dynamic environment move along more complex trajectories. In this condition, a dynamic internal representation of target motion is required. Yet, the nature of such an internal representation has never been investigated. Similarly, the impact of predictive saccades on the predictive smooth pursuit response has never been considered. Therefore, we investigated the predictive smooth pursuit and saccadic responses during the occlusion of a target moving along a circular path. We found that the predictive smooth pursuit was driven by an internal representation of target motion that evolved with time. In addition, we demonstrated that in two dimensions, the predictive smooth pursuit system does influence the amplitude of predictive saccades but not vice versa. In conclusion, in the absence of retinal inputs, the smooth pursuit system is driven by the output of a short-term velocity memory that contains the dynamic representation of target motion.

Neuronal bases of directional expectation and anticipatory pursuit.

Expectation of upcoming events is an essential cognitive function on which anticipatory actions are based. The neuronal basis of this prospective representation is poorly understood. We trained rhesus monkeys in a smooth-pursuit task in which the direction of upcoming target motion was indicated using a color cue. Under these conditions, directional expectation frequently evoked anticipatory smooth movements. We found that the activity of a population of neurons in the supplementary eye fields encoded the expected future direction of the target. Neuronal activity increased after presentation of the cue, indicating future target motion in the preferred direction. Neuronal activity either remained unaltered or was reduced if the antipreferred direction was cued. In addition, ∼30% of these neurons were more active during trials with anticipatory pursuit in the preferred direction than during trials when monkeys did not anticipate target motion onset. This subset of recorded neurons encoded the direction of the subsequent anticipatory pursuit. We hypothesize that the neural representation of directional expectation could be conceptualized as a competitive interaction between pools of neurons representing likely future events, with the winner of this competition determining the direction of the subsequent anticipatory movement. Similar mechanisms could drive prediction before movement initiation in other motor domains.

Smooth eye movements evoked by electrical stimulation of the cat's superior colliculus.

Head-fixed gaze shifts were evoked by electrical stimulation of the deeper layers of the cat superior colliculus (SC). After a short latency, saccades were triggered with kinematics similar to those of visually guided saccades. When electrical stimulation was maintained for more than 150–200 ms, postsaccadic smooth eye movements (SEMs) were observed. These movements were characterized by a period of approximately constant velocity following the evoked saccade. Depending on electrode position, a single saccade followed by a slow displacement or a “staircase” of saccades interspersed by SEMs were evoked. Mean velocity decreased with increasing deviation of the eye in the orbit in the direction of the movement. In the situation where a single evoked saccade was followed by a smooth movement, the duration of the latter depended on the duration of the stimulation train. In the situation where evoked saccades converged towards a restricted region of the visual field (“goal”-directed or craniocentric saccades), the SEMs were directed towards the centre of this region and their mean velocity decreased as the eye approached the goal. The direction of induced SEMs depended on the site of stimulation, as is the case for saccadic eye movements, and was not modified by stimulation parameters (“place” code). On the other hand, mean velocity of the movements depended on the site of stimulation and on the frequency and intensity of the current (“rate” code), as reported for saccades in the cat. The kinematics of these postsaccadic SEMs are similar to the kinematics of slow, postsaccadic correction observed during visually triggered gaze shifts of the alert cat. These results support the hypothesis that the SC is not exclusively implicated in the control of fast refixation of gaze but also in controlling postsaccadic conjugate slow eye movements in the cat.

Shared Brainstem Pathways for Saccades and Smooth-Pursuit Eye Movements

A long‐standing belief holds that the saccadic and smooth‐pursuit eye movement systems are composed of largely separate premotor circuits, at least in the brainstem. One crucial prediction predicated on this belief is that the tonic discharge of omnipause neurons (OPNs), which are thought to be part of only the saccadic system, should not be modulated during pursuit eye movements. This report shows that the discharge of OPNs, in contradiction, is modulated downward during pursuit movements. In contrast to their behavior during saccades, where they pause completely for the duration of the movement, the downward modulation during pursuit did not totally silence OPNs. The depth of the downward modulation was correlated with the speed of the ongoing pursuit movement. Another type of cell, which we have named saccade/pursuit neurons, was recorded in the paramedian pontine reticular formation near the location of OPNs. This subpopulation of burst cells discharged a cascade of spikes for saccades in a preferred direction. They also displayed a lower‐frequency sustained discharge of spikes for the duration of pursuit in the same preferred direction. These data suggest a new type of combined model for the organization of the brainstem saccade/pursuit system. In this new combined model, the OPNs form a common inhibitory mechanism for both types of movements, and the saccade/pursuit neurons participate in the eye‐velocity modulation of OPN discharge or membrane polarization during either type of movement.

How Do Primates Anticipate Uncertain Future Events

The timing of an upcoming event depends on two factors: its temporal position, proximal or distal with respect to the present moment, and the unavoidable stochastic variability around this temporal position. We searched for a general mechanism that could describe how these two factors influence the anticipation of an upcoming event in an oculomotor task. Monkeys were trained to pursue a moving target with their eyes. During a delay period inserted before target motion onset, anticipatory pursuit responses were frequently observed. We found that anticipatory movements were altered by the temporal position of the target. Increasing the timing uncertainty associated with the stimulus resulted in an increase in the width of the latency distribution of anticipatory pursuit. These results show that monkeys relied on an estimation of the changing probability of target motion onset as time elapsed during the delay to decide when to initiate an anticipatory smooth eye movement.

Slow correcting eye movements of head-fixed, trained cats toward stationary targets.

Inspection of eye saccades made by head-fixed, trained cats revealed the existence of many eye shifts at an approximately constant velocity during the deceleratory phase of the saccade or at the end of it. Slow eye movements occurring at the end of a saccade are usually referred to as “postsaccadic drifts”. It is shown that the duration and mean velocity of these “drifts” are related to the amplitude of the movement. The kinematics of these slow eye movements are nevertheless different from those of saccades. Slow movements at the end of the gaze shift have longer durations than those occurring during the intersaccadic interval between a saccade and a reacceleration of the eye. A closer study of the drifts of three trained cats showed that they play an important corrective role in reducing the residual error at the end of a saccade or during an intersaccadic interval. This functional corrective role was demonstrated by relating the amplitude of the slow movement to the amplitude of the residual error when the slow velocity eye shift began. It is therefore proposed to name these eye shifts “slow correcting movements”.

Biological motion drives perception and action

Presenting a few dots moving coherently on a screen can yield to the perception of human motion. This perception is based on a specific network that is segregated from the traditional motion perception network and that includes the superior temporal sulcus (STS). In this study, we investigate whether this biological motion perception network could influence the smooth pursuit response evoked by a point-light walker. We found that smooth eye velocity during pursuit initiation was larger in response to the point-light walker than in response to one of its scrambled versions, to an inverted walker or to a single dot stimulus. In addition, we assessed the proximity to the point-light walker (i.e. the amount of information about the direction contained in the scrambled stimulus and extracted from local motion cue of biological motion) of each of our scrambled stimuli in a motion direction discrimination task with manual responses and found that the smooth pursuit response evoked by those stimuli moving across the screen was modulated by their proximity to the walker. Therefore, we conclude that biological motion facilitates smooth pursuit eye movements, hence influences both perception and action.

Causality Attribution Biases Oculomotor Responses

When viewing one object move after being struck by another, humans perceive that the action of the first object “caused” the motion of the second, not that the two events occurred independently. Although established as a perceptual and linguistic concept, it is not yet known whether the notion of causality exists as a fundamental, preattentional “Gestalt” that can influence predictive motor processes. Therefore, eye movements of human observers were measured while viewing a display in which a launcher impacted a tool to trigger the motion of a second “reaction” target. The reaction target could move either in the direction predicted by transfer of momentum after the collision (“causal”) or in a different direction (“noncausal”), with equal probability. Control trials were also performed with identical target motion, either with a 100 ms time delay between the collision and reactive motion, or without the interposed tool. Subjects made significantly more predictive movements (smooth pursuit and saccades) in the causal direction during standard trials, and smooth pursuit latencies were also shorter overall. These trends were reduced or absent in control trials. In addition, pursuit latencies in the noncausal direction were longer during standard trials than during control trials. The results show that causal context has a strong influence on predictive movements.