The nucleus prepositus predominantly outputs eye movement-related information during passive and active self-motion

Abstract

Maintaining a constant representation of our heading as we move through the world requires the accurate estimate of spatial orientation. As one turns (or is turned) toward a new heading, signals from the semicircular canals are relayed through the vestibular system to higher-order centers that encode head direction. To date, there is no direct electrophysiological evidence confirming the first relay point of head-motion signals from the vestibular nuclei, but previous anatomical and lesion studies have identified the nucleus prepositus as a likely candidate. Whereas burst-tonic neurons encode only eye-movement signals during head-fixed eye motion and passive vestibular stimulation, these neurons have not been studied during self-generated movements. Here, we specifically address whether burst-tonic neurons encode head motion during active behaviors. Single-unit responses were recorded from the nucleus prepositus of rhesus monkeys and compared for head-restrained and active conditions with comparable eye velocities. We found that neurons consistently encoded eye position and velocity across conditions but did not exhibit significant sensitivity to head position or velocity. Additionally, response sensitivities varied as a function of eye velocity, similar to abducens motoneurons and consistent with their role in gaze control and stabilization. Thus our results demonstrate that the primate nucleus prepositus chiefly encodes eye movement even during active head-movement behaviors, a finding inconsistent with the proposal that this nucleus makes a direct contribution to head-direction cell tuning. Given its ascending projections, however, we speculate that this eye-movement information is integrated with other inputs in establishing higher-order spatial representations.

Saccade direction encoding in the primate entorhinal cortex during visual exploration

“…In support of this idea, the lateral dorsal nucleus of the thalamus, which encodes head direction and is important for place-field representation in rodents (33,34), appears to encode eye position in macaques, as previously described (19). Similarly, it has recently been demonstrated that the nucleus prepositus, thought to be an important part of the rodent head-direction network (2), predominantly outputs eye movement-related information in primates (35). The present data, with the identification of SD cells, provide evidence that this analogous neural circuitry may extend to the entorhinal cortex.…”

Hierarchical control of two-dimensional gaze saccades

“…2 Interestingly, Because during the cancellation of the VOR, the gaze is changing but the eyes remain fixed in the orbit, this study suggests that the discharge of those NPH neurons was correlated with eye-in-head position and not with gaze position. Recently, Dale and Cullen (2013) confirm that NPH neurons discharge with eye movements. Therefore, we modeled the neural integrator for the gaze pathway as an eye position integrator in our new architecture.…”

The brain compass: a perspective on how self-motion updates the head direction cell attractor

“…The second explanation offered by Cullen and Taube (2017) is that the ascending signal to the anterior thalamus does not exclusively transmit angular head velocity, but also carries gazerelated signals. This hypothesis stems from the fact that neurons in the macaque nucleus prepositus hypoglossi, one of the pathways from the VN to the anterior thalamus, predominately carries eye-in-head position and velocity information (e.g., Dale and Cullen, 2013). Whereas the role of eye movements in the HD signal remains to be explored, this second explanation offered is also qualitative, without explaining why the contribution of gaze-relative signals can explain the fact that the absence of vestibular signals compromises HD tuning.…”