Jean-Jacques Orban de Xivry

Dissociating the Roles of the Cerebellum and Motor Cortex during Adaptive Learning: The Motor Cortex Retains What the Cerebellum Learns

Adaptation to a novel visuomotor transformation has revealed important principles regarding learning and memory. Computational and behavioral studies have suggested that acquisition and retention of a new visuomotor transformation are distinct processes. However, this dissociation has never been clearly shown. Here, participants made fast reaching movements while unexpectedly a 30-degree visuomotor transformation was introduced. During visuomotor adaptation, subjects received cerebellar, primary motor cortex (M1) or sham anodal transcranial direct current stimulation (tDCS), a noninvasive form of brain stimulation known to increase excitability. We found that cerebellar tDCS caused faster adaptation to the visuomotor transformation, as shown by a rapid reduction of movement errors. These findings were not present with similar modulation of visual cortex excitability. In contrast, tDCS over M1 did not affect adaptation, but resulted in a marked increase in retention of the newly learnt visuomotor transformation. These results show a clear dissociation in the processes of acquisition and retention during adaptive motor learning and demonstrate that the cerebellum and primary motor cortex have distinct functional roles. Furthermore, they show that is possible to enhance cerebellar function using tDCS.

Saccades and pursuit: two outcomes of a single sensorimotor process

Saccades and smooth pursuit eye movements are two different modes of oculomotor control. Saccades are primarily directed toward stationary targets whereas smooth pursuit is elicited to track moving targets. In recent years, behavioural and neurophysiological data demonstrated that both types of eye movements work in synergy for visual tracking. This suggests that saccades and pursuit are two outcomes of a single sensorimotor process that aims at orienting the visual axis.

Temporal discounting of reward and the cost of time in motor control.

Why do movements take a characteristic amount of time, and why do diseases that affect the reward system alter control of movements? Suppose that the purpose of any movement is to position our body in a more rewarding state. People and other animals discount future reward as a hyperbolic function of time. Here, we show that across populations of people and monkeys there is a correlation between discounting of reward and control of movements. We consider saccadic eye movements and hypothesize that duration of a movement is equivalent to a delay of reward. The hyperbolic cost of this delay not only accounts for kinematics of saccades in adults, it also accounts for the faster saccades of children, who temporally discount reward more steeply. Our theory explains why saccade velocities increase when reward is elevated, and why disorders in the encoding of reward, for example in Parkinsons disease and schizophrenia, produce changes in saccade. We show that delay of reward elevates the cost of saccades, reducing velocities. Finally, we consider coordinated movements that include motion of eyes and head and find that their kinematics is also consistent with a hyperbolic, reward-dependent cost of time. Therefore, each voluntary movement carries a cost because its duration delays acquisition of reward. The cost depends on the value that the brain assigns to stimuli, and the rate at which it discounts this value in time. The motor commands that move our eyes reflect this cost of time.

Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia

Selective impairment of face recognition following brain damage, as in acquired prosopagnosia, may cause a dramatic loss of diagnosticity of the eye area of the face and an increased reliance on the mouth for identification (Caldara et al., 2005). To clarify the nature of this phenomenon, we measured eye fixation patterns in a case of pure prosopagnosia (PS, Rossion et al., 2003) during her identification of photographs of personally familiar faces (27 children of her kindergarten). Her age-matched colleague served as a control. Consistent with previous evidence, the normal control identified the faces within two fixations located just below the eyes (central upper nose). This pattern (location and duration) of fixations remained unchanged even by increasing difficulty by presenting anti-caricatures of the faces. In contrast, the great majority of the patients fixations, irrespective of her accuracy, were located on the mouth. Overall, these observations confirm the abnormally reduced processing of the upper area of the face in acquired prosopagnosia. Most importantly, the prosopagnosic patient also fixated the area of the eyes spontaneously in between the first and last fixation, ruling out alternative accounts of her behaviour such as, for example, avoidance or failure to orient attention to the eyes, as observed in autistic or bilateral amygdala patients. Rather, they reinforce our proposal of a high-level perceptual account (Caldara et al., 2005), according to which acquired prosopagnosic patients have lost the ability to represent multiple elements of an individual face as a perceptual unit (holistic face perception). To identify a given face, they focus very precisely on local features rather than seeing the whole of a face from its diagnostic centre (i.e., just below the eyes). The upper area of the face is particularly less attended to and less relevant for the prosopagnosic patient because it contains multiple features that require normal holistic perception in order to be the most diagnostic region. Consequently, prosopagnosic patients develop a more robust representation of the mouth, a relatively isolated feature in the face that may contain more information than any single element of the upper face area, and is thus sampled repeatedly for resolving ambiguity in the process of identification.

Contributions of the Motor Cortex to Adaptive Control of Reaching Depend on the Perturbation Schedule

During adaptation, motor commands tend to repeat as performance plateaus. It has been hypothesized that this repetition produces plasticity in the motor cortex (M1). Here, we considered a force field reaching paradigm, varied the perturbation schedule to potentially alter the amount of repetition, and quantified the interaction between disruption of M1 using transcranial magnetic stimulation (TMS) and the schedule of perturbations. In the abrupt condition (introduction of the perturbation on a single trial followed by constant perturbation), motor output adapted rapidly and was then followed by significant repetition as performance plateaued. TMS of M1 had no effect on the rapid adaptation phase but reduced adaptation at the plateau. In the intermediate condition (introduction of the perturbation over 45 trials), disruption of M1 had no effect on the phase in which motor output changed but again impaired adaptation when performance had plateaued. Finally, when the perturbation was imposed gradually (over 240 trials), the motor commands continuously changed during adaptation and never repeated, and disruption of M1 had no effect on performance. Therefore, TMS of M1 appeared to reduce adaptation of motor commands during a specific phase of learning: when motor commands tended to repeat.

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.

Stimulation of the Human Motor Cortex Alters Generalization Patterns of Motor Learning

It has been hypothesized that the generalization patterns that accompany learning carry the signatures of the neural systems that are engaged in that learning. Reach adaptation in force fields has generalization patterns that suggest primary engagement of a neural system that encodes movements in the intrinsic coordinates of joints and muscles, and lesser engagement of a neural system that encodes movements in the extrinsic coordinates of the task. Among the cortical motor areas, the intrinsic coordinate system is most prominently represented in the primary sensorimotor cortices. Here, we used transcranial direct current stimulation (tDCS) to alter mechanisms of synaptic plasticity and found that when it was applied to the motor cortex, it increased generalization in intrinsic coordinates but not extrinsic coordinates. However, when tDCS was applied to the posterior parietal cortex, it had no effects on learning or generalization in the force field task. The results suggest that during force field adaptation, the component of learning that produces generalization in intrinsic coordinates depends on the plasticity in the sensorimotor cortex.

Kalman Filtering Naturally Accounts for Visually Guided and Predictive Smooth Pursuit Dynamics

The brain makes use of noisy sensory inputs to produce eye, head, or arm motion. In most instances, the brain combines this sensory information with predictions about future events. Here, we propose that Kalman filtering can account for the dynamics of both visually guided and predictive motor behaviors within one simple unifying mechanism. Our model relies on two Kalman filters: (1) one processing visual information about retinal input; and (2) one maintaining a dynamic internal memory of target motion. The outputs of both Kalman filters are then combined in a statistically optimal manner, i.e., weighted with respect to their reliability. The model was tested on data from several smooth pursuit experiments and reproduced all major characteristics of visually guided and predictive smooth pursuit. This contrasts with the common belief that anticipatory pursuit, pursuit maintenance during target blanking, and zero-lag pursuit of sinusoidally moving targets all result from different control systems. This is the first instance of a model integrating all aspects of pursuit dynamics within one coherent and simple model and without switching between different parallel mechanisms. Our model suggests that the brain circuitry generating a pursuit command might be simpler than previously believed and only implement the functional equivalents of two Kalman filters whose outputs are optimally combined. It provides a general framework of how the brain can combine continuous sensory information with a dynamic internal memory and transform it into motor commands.

Changes in corticospinal excitability during reach adaptation in force fields

Both abrupt and gradually imposed perturbations produce adaptive changes in motor output, but the neural basis of adaptation may be distinct. Here, we measured the state of the primary motor cortex (M1) and the corticospinal network during adaptation by measuring motor-evoked potentials (MEPs) before reach onset using transcranial magnetic stimulation of M1. Subjects reached in a force field in a schedule in which the field was introduced either abruptly or gradually over many trials. In both groups, by end of the training, muscles that countered the perturbation in a given direction increased their activity during the reach (labeled as the on direction for each muscle). In the abrupt group, in the period before the reach toward the on direction, MEPs in these muscles also increased, suggesting a direction-specific increase in the excitability of the corticospinal network. However, in the gradual group, these MEP changes were missing. After training, there was a period of washout. The MEPs did not return to baseline. Rather, in the abrupt group, off direction MEPs increased to match on direction MEPs. Therefore, we observed changes in corticospinal excitability in the abrupt but not gradual condition. Abrupt training includes the repetition of motor commands, and repetition may be the key factor that produces this plasticity. Furthermore, washout did not return MEPs to baseline, suggesting that washout engaged a new network that masked but did not erase the effects of previous adaptation. Abrupt but not gradual training appears to induce changes in M1 and/or corticospinal networks.

Review of the major findings about Duane retraction syndrome (DRS) leading to an updated form of classification

In view of all the reported evidence by electromyography in the 1970s, by histology in the 1980s, and by cerebral imagery since the 2000s, Duane retraction syndrome (DRS) has been described as the consequence of a congenital anomaly of the 6th cranial nerve nuclei with aberrant innervations by supply from the 3rd cranial nerve. Both genetic and environmental factors are likely to play a role when the cranial nerves and ocular muscles are developing between the 4th and the 8th week of gestation. New data from eye movement recordings contributed to better understanding the binocular control of saccades. Modeling of saccades in DRS seems promising for the quantification of the innervational deficit and the mechanical properties of the eye plant. The usual clinical classification of DRS needs to be updated in order to match more accurately the underlying dysinnervation of the extra ocular muscles and to illustrate the continuum that exists between the various forms. This review aims to summarize the major findings about DRS and to guide the clinician in the surgical management of this particular form of strabismus.