Jefferson E. Roy

Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

The ability to distinguish sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. To accomplish this, it has been proposed that an internal prediction of the consequences of our actions is compared with the actual sensory input to cancel the resultant self-generated activation. Here, we provide evidence for this hypothesis at an early stage of processing in the vestibular system. Previous studies have shown that neurons in the vestibular nucleus, which receive direct inputs from vestibular afferent fibers, are responsive to passively applied head movements. However, these same neurons do not reliably encode head velocity resulting from self-generated movements of the head on the body. In this study, we examined the mechanism that underlies the selective elimination of vestibular sensitivity to active head-on-body rotations. Individual neurons were recorded in monkeys making active head movements. The correspondence between intended and actual head movement was experimentally controlled. We found that a cancellation signal was gated into the vestibular nuclei only in conditions in which the activation of neck proprioceptors matched that expected on the basis of the neck motor command. This finding suggests that vestibular signals that arise from self-generated head movements are inhibited by a mechanism that compares the internal prediction of the sensory consequences by the brain to the actual resultant sensory feedback. Because self-generated vestibular inputs are selectively cancelled early in processing, we propose that this gating is important for the computation of spatial orientation and control of posture by higher-order structures.

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).

Passive activation of neck proprioceptive inputs does not influence the discharge patterns of vestibular nuclei neurons

Position-vestibular-pause (PVP) neurons and vestibular only (VO) neurons are thought to mediate the vestibulo-ocular and vestibulo-collic reflexes, respectively. Both neuron classes are much less sensitive to head motion during active gaze shifts than during passive whole-body rotation (pWBR).1–5 The mechanism that underlies this differential processing of vestibular information is not known. Neck muscle proprioceptive inputs have been proposed to contribute to the observed attenuation. While experiments in decerebrate animals have shown that neck proprioception can modulate the responses of vestibular neurons,6,7 studies in alert monkeys have reported varying degrees of influence.3,8–10 However, these latter studies assumed that the monkey did not generate a neck motor command during the paradigms used to evaluate neck proprioceptive inputs. Since a coincident neck efference command could effect neuron discharges, in this study we measured the torque produced during passive rotation of the body relative to a stationary head, thereby allowing us to dissociate the effect of neck proprioception from efference commands. The discharge activity of vestibular neurons in three rhesus monkeys was initially recorded during voluntary eye movements and pWBR with the monkeys in the headrestrained condition. After a neuron was fully characterized, the monkey’s head was slowly and carefully released, allowing free rotation of its head through its natural range of motion. The response of the same neuron was then recorded during the voluntary head movements made during combined eye-head gaze shifts (15° to 65°). In agreement with previous studies, the head velocity sensitivities of PVP (n = 17) and VO (n = 40) neurons were significantly attenuated during gaze shifts as compared to those estimated during pWBR (mean sensitivity (± SEM) = 0.37± 0.17 vs. 1.31± 0.13 (spk/s)/(deg/s), and 0.17± 0.03 vs. 0.53± 0.04 (spk/s)/(deg/s), for PVP and VO neurons, respectively; FIG. 1E and F, compare white and gray-shaded columns). The influence of neck proprioceptive inputs on vestibular neurons was first tested by passively rotating the monkeys’ bodies while their heads were held earth-station-

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-