Discharge patterns and recruitment order of identified motoneurons and internuclear neurons in the monkey abducens nucleus

Abstract

1. Single neurons in the abducens nucleus were recorded extracellularly in alert rhesus macaques trained to make a variety of eye movements. An abducens neurons was identified as a motoneuron (MN) if its action potentials triggered an averaged EMG potential in the lateral rectus muscle. Abducens internuclear neurons (INNs) that project to the oculomotor nucleus were identified by collision block of spontaneous with antidromic action potentials evoked with a stimulating electrode placed in the medial rectus subdivision of the contralateral oculomotor nucleus. 2. All abducens MNs and INNs had qualitatively similar discharge patterns consisting of a burst of spikes for lateral saccades and a steady firing whose rate increased with lateral eye position in excess of a certain threshold. 3. For both MNs and INNs the firing rates associated with different, constant eye positions could be described accurately by a straight line with slope, K (the eye position sensitivity in spikes.s-1.deg-1), and intercept, T (the eye position threshold for steady firing). For different MNs, K increased as T varied from more medial to more lateral values. In contrast, the majority of INNs already were active for values of T more medial than 20 degrees and showed little evidence of recruitment according to K. 4. During horizontal sinusoidal smooth-pursuit eye movements, both MNs and INNs exhibited a sinusoidal modulation in firing rate whose peak preceded eye position. From these firing rate patterns, the component of firing rate related to eye velocity, R (the eye velocity sensitivity in spikes.s-1.deg-1.s-1), was determined. The R for INNs was, on average, 78% larger than that for MNs. Furthermore, R increased with T for MNs, whereas INNs showed no evidence of recruitment according to R. If, as in the cat, the INNs of monkeys provide the major input to medial rectus MNs and if simian medial rectus MNs behave like our abducens MNs, then recruitment order, which is absent in INNs, must be established at the MN pool itself. 5. Unexpectedly, the R of MNs decreased with the frequency of the smooth-pursuit movement. Furthermore, the eye position sensitivity, K, obtained during steady fixations was usually less than that determined during smooth pursuit. Therefore, conclusions about the roles of MNs and premotor neurons based on how their R and K values differ must be viewed with caution if the data have been obtained under different tracking conditions.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

“…Muscle force measurements also better reflect the high-frequency behavior of motoneurons than eye position measurements, which are low-pass filtered by the viscous orbit (60~100 Hz, Bahill et al 1981). Another limitation of the study was that we were unable to identify whether a recorded abducens neuron was a motoneuron that innervates the lateral rectus muscle or an internuclear neuron that projects to the contralateral oculomotor nucleus (Langer et al 1986;Zhou and King 1998;Clendaniel and Mays 1994;Gamlin et al 1989;Fuchs et al 1988;Sylvestre and Cullen 2002). It was likely that our population consisted of neurons from both groups.…”

“…Briefly, a stainless steel cylinder was implanted stereotaxically, and a tungsten microelectrode was advanced through a 21-gauge guide cannula by a motorized microdrive. The abducens nucleus was identified by the characteristic tonal quality of the background activity as heard on the audio monitor (Fuchs et al 1988;Robinson 1970). We included in our sample only the neurons that were recorded concurrently with the characteristic background activity of the abducens nucleus.…”

Morphology, Intrinsic Membrane Properties, and Rotation-Evoked Responses of Trochlear Motoneurons in the Turtle

“…In these studies, synaptic responses were evoked by electrical stimulation of afferent pathways when they were examined at all. As a rule, studies of the VOR employing natural stimulation have been restricted to extracellular recording (Blanks et al 1978;Delgado-Garcia et al 1986;Fuchs et al 1988;Pastor and Gonzalez-Forero 2003;Pastor et al 1991).…”

“…In these studies, synaptic responses were evoked by electrical stimulation of afferent pathways when they were examined at all. As a rule, studies of the VOR employing natural stimulation have been restricted to extracellular recording (Blanks et al 1978;Delgado-Garcia et al 1986;Fuchs et al 1988; Pastor and Gonzalez-Forero 2003; Pastor et al 1991).Our laboratory is studying vestibuloocular physiology using an in vitro preparation consisting of the intact brain stem of the pond turtle with attached temporal bones (Ariel et al 2004;Fan et al 1997;Jones and Ariel 2006). Because of the extraordinary resistance to hypoxia exhibited by the turtle, the brain can be isolated in this fashion, facilitating the use of intracellular recording techniques.…”

System Identification From Multiple Short-Time-Duration Signals

“…The modeling of the oculomotor plant dynamics is important for a number of reasons, including relating eye movement to oculomotor firing patterns [10], [11] and also for understanding the underlying algorithms governing eye-movement control [12], [13].…”