Pierre A. Sylvestre

Premotor Correlates of Integrated Feedback Control for Eye–Head Gaze Shifts

Simple activities like picking up the morning newspaper or catching a ball require finely coordinated movements of multiple body segments. How our brain readily achieves such kinematically complex yet remarkably precise multijoint movements remains a fundamental and unresolved question in neuroscience. Many prevailing theoretical frameworks ensure multijoint coordination by means of integrative feedback control. However, to date, it has proven both technically and conceptually difficult to determine whether the activity of motor circuits is consistent with integrated feedback coding. Here, we tested this proposal using coordinated eye–head gaze shifts as an example behavior. Individual neurons in the premotor network that command saccadic eye movements were recorded in monkeys trained to make voluntary eye–head gaze shifts. Head-movement feedback was experimentally controlled by unexpectedly and transiently altering the head trajectory midflight during a subset of movements. We found that the duration and dynamics of neuronal responses were appropriately updated following head perturbations to preserve global movement accuracy. Perturbation-induced increases in gaze shift durations were accompanied by equivalent changes in response durations so that neuronal activity remained tightly synchronized to gaze shift offset. In addition, the saccadic command signal was updated on-line in response to head perturbations applied during gaze shifts. Nearly instantaneous updating of responses, coupled with longer latency changes in overall discharge durations, indicated the convergence of at least two levels of feedback. We propose that this strategy is likely to have analogs in other motor systems and provides the flexibility required for fine-tuning goal-directed movements.

Signal Processing by Vestibular Nuclei Neurons Is Dependent on the Current Behavioral Goal

Abstract: The vestibular sensory apparatus and associated vestibular nuclei are generally thought to encode angular head velocity during our daily activities. However, in addition to direct inputs from vestibular afferents, the vestibular nuclei receive substantial projections from cortical, cerebellar, and other brainstem structures. Given this diversity of inputs, the question arises: How are the responses of vestibular nuclei neurons to head velocity modified by these additional inputs during naturally occurring behaviors? Here we have focused on the signal processing done by two specific classes of neurons in the vestibular nuclei: (1) position‐vestibular‐pause (PVP) neurons that mediate the vestibulo‐ocular reflex (VOR), and (2) vestibular‐only (VO) neurons that are thought to mediate, at least in part, the vestibulo‐collic reflex (VCR).

Do extraocular motoneurons encode head velocity during head-restrained versus head-unrestrained saccadic and smooth pursuit movements?

Microstimulation experiments in the superior colliculus1 and single-unit recordings from its target, the premotor saccadic burst neurons2 (SBNs, located in the paramedian pontine reticular formation), have shown that the saccadic burst generator encodes head as well as eye movements during head-unrestrained gaze shifts. There is also evidence suggesting that premotor circuits likely encode eye and head motion during head-unrestrained gaze pursuit.3,4 Hence, although extraocular muscle motoneurons directly drive the eye movements, the premotor inputs they receive during voluntary gaze redirection behaviors are related to eye and head motion. To account for this apparent mismatch in premotor/motor drives during head-unrestrained movements, two mechanisms have been envisaged: (1) a premotor signal proportional to the head contribution of the gaze shift is subtracted out at the level of the motoneurons, or (2) individual motoneurons encode eye and head motor commands, and proper eye movements result from interactions at the level of the oculomotor plant. Rather surprisingly, previous metric-based studies of extraocular motoneuron discharges during gaze shifts have suggested that the latter mechanism may be more appropriate.5,6 Here, we have characterized the firing rates of extraocular motoneurons in head-restrained and head-unrestrained conditions using a more sophisticated dynamic-based approach and find that metric-based analyses can yield misleading results. As we have previously shown, the firing rates of extraocular motoneurons and internuclear neurons in the abducens nucleus (collectively referred to as ABNs) during head-restrained eye movements could be well approximated using a first-order dynamic model of eye motion.7 In the present study, we characterized and compared the discharge dynamics of the same isolated ABNs (n = 7, obtained from two trained rhesus monkeys) during (1) head-restrained saccades versus head-unrestrained gaze shifts, and (2) head-restrained smooth pursuit versus head-unrestrained gaze pursuit. We first observed that the activity of ABNs, in contrast to that of SBNs, remains related to the eye motion by the same dynamic relationship during head-restrained saccades and head-unrestrained gaze shifts.5 This is illustrated in FIGURE 1A (head-