Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons

Abstract

Saccadic burst neurons in the pontine reticular formation have been implicated in the generation of saccades in the horizontal plane on the basis of lesion and extracellular recording studies in the cat and monkey. In the present study, saccadic burst neurons were anatomically and physiologically characterized with intraaxonal recording and injection of horseradish peroxidase in the alert squirrel monkey. A population of burst neurons were found that appear analogous to the excitatory burst neurons (EBNs) described previously in the cat. All neurons are located in the caudal pontine reticular formation and have a major axonal projection to the ipsilateral abducens nucleus. Additional projections were found to the medial vestibular nucleus, the nucleus prepositus, and regions of the pontine and medullary reticular formation rostral, ventral, and caudal to the abducens. All neurons fire exclusively during saccades and have a discharge pattern similar to that of medium-lead burst neurons described previously in the cat and monkey. In most neurons the saccadic burst begins 5-15 msec before saccade onset. Linear relationships exist between burst duration and saccade duration, number of spikes in the burst and saccade amplitude, and firing frequency and instantaneous velocity. Physiological activity of each neuron shows the closest relationship with the amplitude of the saccade component in a particular direction. For all neurons, this on-direction is in the ipsilateral hemifield and is predominantly horizontal, but may have either an upward or downward vertical component. These results support a major role for the EBNs in the monkey in generating the saccadic burst in abducens motoneurons, as well as in contributing to the oculomotor activity in other classes of premotor neurons.

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

“…The participation of neurons with saccade-related bursts in the control of eye movements is well documented (see Sparks 2002 for a review). At least a subset of these cells, excitatory burst neurons (EBNs), projects directly to the ipsilateral abducens nucleus (Strassman et al 1986) and discharges a number of spikes directly proportional to the amplitude of the horizontal component of a saccade (Keller 1974). The eye movement evoked by stimulation of the PPRF region in the head-restrained monkey is consistent with EBN activity: for a fixed current intensity and frequency, the amplitude of the movement is proportional to the number of stimulation pulses (Cohen and Komatsuzaki 1972).…”

“…The abducens nuclei were identified by their burst-tonic activity associated with saccades (Schiller 1970) and by the effects of stimulation (Reinhart and Zuber 1970). The PPRF was identified by its location with respect to the abducens nuclei (Strassman et al 1986), the effects of stimulation (Cohen and Komatsuzaki 1972), and the discharge characteristics during head-restrained saccades (Keller 1974) and head-unrestrained gaze shifts (Whittington et al 1984;Ling et al 1999;Sylvestre and Cullen 2006). Stimulation was applied on penetrations that spanned anterior from the rostral pole of the abducens nucleus by 3.5 mm in one animal and 1.0 mm in the second.…”

“…In fact, a head movement without an accompanying gaze shift is typically initiated during prolonged stimulation of the omnipause neurons prior to gaze onset (Gandhi and Sparks 2007). Also, intra-axonal injections of physiologically characterized EBNs in the squirrel monkey did not reveal axons that extend beyond the prepositus (Strassman et al 1986), although a polysynaptic connection cannot be excluded. Finally, some component of the observed head movement could have resulted from modulation of neck muscle activity as the eyes were driven to increasingly ipsilateral positions in the orbits (Vidal et al 1982;Andre-Deshays et al 1988;Corneil et al 2002;Wang et al 2007).…”

Optogenetic Localization and Genetic Perturbation of Saccade-Generating Neurons in Zebrafish

“…Both types of burst neurons directly synapse with the abducens motor neurons (Yoshida et al, 1982). The EBNs project to the ipsilateral abducens nucleus to excite agonist motor neurons (Strassman et al, 1986a), whereas the IBNs inhibit antagonist motor neurons in the contralateral abducens nucleus (Strassman et al, 1986b). Together, this activation pattern results in a quick, synchronous (conjugate) movement of both eyes in the same direction.…”

A physiological study of vestibular and prepositus hypoglossi neurones projecting to the abducens nucleus in the alert cat.

“…in the set of brainstem neurones projecting monosynaptically on ocular motoneurones. The main afferent inputs to ABD neurones are organized in reciprocal excitatory and inhibitory synaptic connections (Escudero & Delgado-Garcia, 1988) arising from (i) the ipsilateral excitatory (Kaneko, Evinger & Fuchs, 1981;Strassman, Highstein & McCrea, 1986a) and the contralateral inhibitory burst neurones (Hikosaka, Igusa, Nakao & Shimazu, 1978b;Yoshida, McCrea, Berthoz & Vidal, 1982;Strassman, Highstein & McCrea, 1986b), located in the pontomedullary reticular formation; (ii) the contralateral excitatory and ipsilateral inhibitory medial vestibular neurones (Baker, Mano & Shimazu, 1969;Hikosaka, Nagao & Shimazu, 1980;McCrea, Yoshida, Berthoz & 540 VESTIBULAR AND PREPOSITUS AFFERENTS TO ABDUCENS 541 Baker, 1980;Berthoz, Droulez, Vidal & Yoshida, 1989); and (iii) the ipsilateral excitatory and contralateral inhibitory prepositus hypoglossi (PH) neurones (Escudero & Delgado-Garcia, 1988;Spencer, Wenthold & Baker, 1989).…”