Coordination of gaze shifts in primates: Brainstem inputs to neck and extraocular motoneuron pools

Abstract

To determine whether there are brainstem regions that provide common input to the motoneurons that move both the head and the eyes, we injected wheat germ agglutinin-horseradish peroxidase complex (WGA-HRP) into neck motoneuron pools at spinal level C2 (N = 3) and extraocular motoneuron pools in the abducens (N = 1) and oculomotor/trochlear (N = 1) nuclei of rhesus and fascicularis macaques. We also injected WGA-HRP into spinal level C5-7 (N = 1) of a fascicularis macaque for comparison. After injections into C2, we observed retrogradely labeled cells in the ventral reticular formation (NRV), the gigantocellular reticular formation (NRG), and both the oral (NRPO) and the caudal (NRPC) divisions of the paramedian pontine reticular formation (PPRF). There was also a column of labeled cells in the cuneate reticular nucleus (NCUN) just lateral to the ipsilateral periaqueductal gray (PAG). This column extended rostrally into the central mesencephalic reticular formation (CMRF). In addition, there were labeled cells in the region ventral and caudal to the rostral interstitial nucleus of the MLF (riMLF), the area lateral to the interstitial nucleus of Cajal (INC), and the ventral part of the lateral vestibular nucleus (LVN) and lateral part of the medial vestibular nucleus (MVN). There were also a few labeled cells in the fastigial (FN) and interposed (IN) nuclei of the cerebellum but very few in the superior colliculus (SC). In contrast, the injection into C5-7 labeled many cells in the lateral vestibular nucleus (LVN) and very few in FN or IN. Injecting WGA-HRP into the abducens nucleus and the surrounding tissue labeled many cells in SC, PPRF, MVN, FN, and nucleus prepositus hypoglossi (NPH). Injecting into the oculomotor/trochlear nuclei and nearby tissue labeled cells in SC, INC, riMLF, FN, IN, MVN, and superior vestibular nucleus (SVN). Structures that project to both neck and eye motoneuron pools, and therefore probably participate in both head and eye movements, include the lateral part of the MVN and both NRPO and NRPC in the PPRF. Those that project primarily to neck motoneurons in C2 include the NRV, the NRG, and the NCUN-CMRF column. Those projecting exclusively to extraocular nuclei include the NPH, INC, riMLF, NRPD, and SC. We use these data to propose a scheme for control of combined eye-head movements in monkeys.

Head-Unrestrained Gaze Shifts After Muscimol Injection in the Caudal Fastigial Nucleus of the Monkey

“…This observation suggests that in primates, the cFN output essentially influences an oculomotor stage for the control of gaze accuracy, i.e., a functional stage which is situated after that gaze-related commands are decomposed into premotor commands for moving the eyes in the orbit and premotor commands for moving the head. This hypothesis is consistent with an anatomical study showing that fastigial neurons projecting to the peri-abducens region are located more caudally than those projecting to the neck motoneurons pool in the upper cervical C2 (Robinson et al 1994). Thus the fastigial control of gaze shifts would involve different path-ways for controlling the eye and head components of gaze shifts.…”

“…This independent control of eye and head movements by the fastigial nucleus is also corroborated by results from two other studies. First, an anatomic study showed that fastigial neurons projecting to the peri-abducens region are located more caudally than those projecting to the neck motoneurons pool in the upper cervical C 2 (Robinson et al 1994). Second, during electrical microstimulation of the fastigial oculomotor region, saccadic eye movements were mostly evoked and rarely accompanied with head movements (Quinet and Goffart 2007).…”

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

“…In contrast to the PPRF data, stimulation of certain regions of the nucleus reticularis gigantocellularis (NRG) produces movements (Sprague and Chambers 1954;Quessy and Freedman 2004;Sasaki et al 2004) with an attenuated VOR gain (Quessy and Freedman 2004). The NRG resides caudal to the abducens nucleus (Peterson et al 1975;Tohyama et al 1979;Huerta and Harting 1982;Robinson et al 1994) and, compared to the PPRF, has a higher density of projections to the neck motoneurons (Tohyama et al 1979;Grantyn and Berthoz 1988). Quessy and Freedman (2004) assumed that they activated neurons within the pathway controlling only head movements and, therefore, interpreted the observed eye movement as VOR gain readout.…”

“…One possibility is that stimulation recruited fibers that traverse through the PPRF region and relay projections to the neck motoneurons (e.g., May and Porter 1992;Warren et al 2008). Another candidate is a subset of reticulospinal neurons that reside in the PPRF region Robinson et al 1994). Scudder et al (2002) proposed that long-lead burst neurons (LLBNs), which are intermingled with the EBNs, may be involved in controlling both eye and head movements.…”

Synaptic Control of Motoneuronal Excitability

“…Premotor neurons to the abducens and trochlear motor nuclei are also in the pontine reticular formation (699,1115,1344,1420). All three motor nuclei receive input from the vestibular nuclei as part of the vestibulo-ocular reflex (225,341,434,685,699,943,1051,1283). Some of these premotor neurons are GABAergic (superior vestibular nucleus) or cholinergic (the medial vestibular nucleus; Refs.…”