Vergence Neurons Identified in the Rostral Superior Colliculus Code Smooth Eye Movements in 3D Space

Abstract

The rostral superior colliculus (rSC) encodes position errors for multiple types of eye movements, including microsaccades, small saccades, smooth pursuit, and fixation. Here we address whether the rSC contributes to the development of neural signals that are suitable for controlling vergence eye movements. We use both single-unit recording and microstimulation techniques in monkey to answer this question. We found that vergence eye movements can be evoked using microstimulation in the rSC. Moreover, among the previously described neurons in rSC, we recorded a novel population of neurons that either increased (i.e., convergence neurons) or decreased (i.e., divergence neurons) their activity during vergence eye movements. In particular, these neurons dynamically encoded changes in vergence angle during vergence tracking, fixation in 3D space and the slow binocular realignment that occurs after disconjugate saccades, but were completely unresponsive during conjugate or the rapid component of disconjugate saccades (i.e., fast vergence) and conjugate smooth pursuit. Together, our microstimulation and single-neuron results suggest that the SC plays a role in the generation of signals required to precisely align the eyes toward targets in 3D space. We propose that accurate maintenance of 3D eye position, critical for the perception of stereopsis, may be mediated via the rSC.

A central mesencephalic reticular formation projection to the Edinger–Westphal nuclei

“…However, there is some evidence from work in cats that the rostral superior colliculus might modulate lens accommodation (Ohtsuka and Sato 1997; Ohtsuka and Nagasaka 1999). More recently, stimulation of the rostral pole of the superior colliculus was shown to modulate vergence movements in monkeys (Chaturvedi and Van Gisbergen 2000) and cells whose activity is modulated with respect to vergence eye movements have been recorded (Van Horn et al 2013). In addition, pupillary dilation has been recorded following electrical stimulation of the superior colliculus (Wang et al 2014).…”

Strabismus and the Oculomotor System: Insights from Macaque Models

“…A complementary, yet unidentified, pathway likely provides a strabismus signal to the lateral rectus muscle. Recent studies in normal monkeys have suggested that the rostral superior colliculus plays a part in vergence eye movements, and a pathway from the rostral superior colliculus to the abducens nucleus has been hypothesized as providing a slow vergence signal to the LR muscle (Van Horn et al 2013). This pathway could potentially provide the strabismus signal to the LR muscle.…”

Internal organization of medial rectus and inferior rectus muscle neurons in the C group of the oculomotor nucleus in monkey

“…In monkey only injections into the ventral pretectum including the deep layers of the rostral superior colliculus (SC) gave rise to strong anterograde labeling in the LVC, AM, SOA with EWpg, and the C group (B€ uttner-Ennever et al, 1996). This projection may originate from vergence-related neurons in the pretectum (Judge and Cumming, 1986) or from the rostral SC, which is important for eye fixation (Suzuki et al, 2004;van Horn et al, 2013). In monkey and cat, the rostral SC contains neurons whose activity is linked to vergence (van Horn et al, 2013) and accommodation (Suzuki et al, 2004), indicating a role in the linkage of fixation, accommodation, and vergence as required for aligning the eyes during fixation on a visual target.…”