1. Neurons in the superior colliculus (SC) of anesthetized paralyzed squirrel monkeys were injected intracellularly with horseradish peroxidase (HRP) to establish a morphological classification of tectal efferent neurons in this species. These neurons were physiologically identified by their antidromic responses following stimulation of the contralateral predorsal bundle or SC. These cells also responded with postsynaptic potentials to stimulation of the ipsilateral substantia nigra and cerebral peduncle and the contralateral tectum. 2. Quantitative light microscopic analysis of the somatodendritic profiles and axonal trajectories of 27 recovered cells revealed the existence of three major groups of tectal efferent neurons: L (n = 7), X (n = 8), and T (n = 12). 3. L neurons are small or medium size cells with relatively elaborate dendritic trees and are located mainly in the superficial layers of the SC. They participate in the ipsilateral descending and dorsal ascending tectofugal bundles. Intrinsic collaterals of L axons deploy a large number of boutons both near the parent cell body and more ventrally within the deeper tectal layers. 4. X neurons are mostly large in size and multipolar in shape with relatively complex dendritic trees. Their cell bodies are situated mainly in the stratum griseum intermedium and occasionally in the stratum opticum. Axons of X neurons participate in the crossed descending and ipsilateral ventral ascending projections of the SC. In addition, the axonal system of about half of the X neurons includes recurrent collaterals. 5. T neurons are located mainly in the ventral stratum opticum and the dorsal stratum griseum intermedium. They have small or medium-sized, trapezoid or ovoid cell bodies and relatively simple radiating or vertical dendritic trees. Their axons usually participate in two of the major tectofugal bundles besides providing a commissural component and recurrent collaterals. 6. Morphological details revealed in the present study support the notion that distinct tectofugal axonal systems originate from efferent neurons of the primate SC that differ both as to their location in the tectum as well as the appearance of their somata and dendritic trees. The resulting morphological classification of tectal efferent cells provides a framework for the analysis of tectal function in terms of populations of identified neurons.

The anatomical characteristics of vestibular neurons, which are involved in controlling the horizontal vestibulo-ocular reflex, were studied by injecting horseradish peroxidase (HRP) into neurons whose response during spontaneous eye movements had been characterized in alert squirrel monkeys. Most of the vestibular neurons injected with HRP that had axons projecting to the abducens nucleus or the medial rectus subdivision of the oculomotor nucleus had discharge rates related to eye position and eye velocity. Three morphological types of cells were injected whose firing rates were related to horizontal eye movements. Two of the cell types were located in the ventral lateral vestibular nucleus and the ventral part of the medial vestibular nucleus (MV). These vestibular neurons could be activated at monosynaptic latencies following electrical stimulation of the vestibular nerve; increased their firing rate when the eye moved in the direction contralateral to the soma; had tonic firing rates that increased when the eye was held in contralateral positions; and had a pause in their firing rate during saccadic eye movements in the ipsilateral or vertical directions. Eleven of the above cells had axons that arborized exclusively on the contralateral side of the brainstem, terminating in the contralateral abducens nucleus, the dorsal paramedian pontine reticular formation, the prepositus nucleus, medial vestibular nucleus, dorsal medullary reticular formation, caudal interstitial nucleus of the medial longitudinal fasciculus, and raphé obscurus. Eight of the cells had axons that projected rostrally in the ascending tract of Deiters and arborized exclusively on the ipsilateral side of the brainstem, terminating in the ipsilateral medial rectus subdivision of the oculomotor nucleus and, in some cases, the dorsal paramedian pontine reticular formation or the caudal interstitial nucleus of the medial longitudinal fasciculus. Two MV neurons were injected that had discharge rates related to ipsilateral eye position, generated bursts of spikes during saccades in the ipsilateral direction, and paused during saccades in the contralateral direction. The axons of those cells arborized ipsilaterally, and terminated in the ipsilateral abducens nucleus, MV, prepositus nucleus, and the dorsal medullary reticular formation. The morphology of vestibular neurons that projected to the abducens nucleus whose discharge rate was not related to eye movements, or was related primarily to vertical eye movements, is also briefly presented.

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.

Electrophysiological and intracellular labelling studies in the cat have identified a population of saccadic burst neurons in the medullary reticular formation that have an inhibitory, monosynaptic projection to the contralateral abducens nucleus. In the present study, intraaxonal recording and injection of horseradish peroxidase were used to identify and characterize the corresponding population of inhibitory burst neurons (IBNs) in the alert squirrel monkey. Squirrel monkey IBNs are located in the reticular formation ventral and caudal to the abducens nucleus and project contralaterally to the abducens. Additional contralateral projections are present to the vestibular nuclei, the nucleus prepositus, and the pontine and medullary reticular formation rostral and caudal to the abducens. All neurons fire a burst of spikes during saccades and are silent during fixation. In most neurons the burst begins 5-15 msec before saccade onset. The number of spikes in the saccadic burst is linearly related to the amplitude of the component of the saccade in the neuron's on-direction. Linear relationships also exist between burst duration and saccade duration and between firing frequency and instantaneous eye velocity. For all neurons, the on-direction is in the ipsilateral hemifield, with a vertical component that may be either upward or downward. Neurons with projections to the vertically related descending and superior vestibular nuclei tend to have on-directions with larger vertical components than neurons that lack these projections. These results, together with those on excitatory burst neurons reported in the preceding paper, demonstrate a reciprocal organization of burst neuron input to the abducens in the monkey similar to that found in the cat and indicate a major role for these neurons in generating the oculomotor activity in motoneurons as well as in other classes of premotor neurons.

1. In the present study we examine the response of the semicircular canal of the toadfish (Opsanus tau) to head rotation and to mechanical indentation of the membranous labyrinth. The relationship between the two stimuli is described by a new elastohydrodynamic model that delineates the three-dimensional (3-D) spatiotemporal distribution of endolymph pressure and flow. In vivo electrophysiological recordings of primary afferents supplying the horizontal canal (HC) were employed to validate the model predictions. Data were collected from 213 afferents in 18 fish during independent head rotation. HC indentation, utricle (U) indentation, and paired stimuli. To quantify the afferent response and the relationship between the applied sinusoidal stimuli, the magnitude (gain) and temporal relationship (phase) of the first harmonic of modulation were calculated and compared with theoretical predictions. 2. A mathematical based extensively on the 3-D morphology of a toadfish labyrinth and the physical properties of endolymph is presented to describe the relationship between head rotation and mechanical indentation. All model parameters specifying labyrinthine morphology and physical properties of endolymph are known; the model contains no free parameters. New results are independent of the structural properties of the cupula. The analysis employs an asymptotic solution of the Navier-Stokes equations in the three toroidal ducts that includes the 3-D fluid-structure interaction taking place within the enlarged ampulla. The solution addresses the differential pressure (delta P) acting across the cupula and the dilatational pressure acting on both sides of the cupula. The analysis quantifies the hydrodynamics of the HC for mechanical indentations of the long and slender portion of the canal duct (HC indentation) and the U (U indentation). Results specifically relate the indentation stimuli to head rotation. Linear commutations of HC indentation, U indentation, and rotation stimuli are analyzed by matching delta P acting across the cupula for the three stimulus modalities. 3. HC afferents show a linear correspondence between HC indentation, U indentation, and rotation stimuli. Specific experimental results for sinusoidal stimuli at frequencies < 2 Hz show 1) +/- 1 micron-HC indentation commutates with +/- 4 degrees/s rotation, 2) + 1-micron HC indentation commutates with -/+ 15-microns U indentation, and 3) -/+ 15-microns U indentation commutates with +/- 4 degrees/s rotation. These results were obtained by adjusting the relative amplitude and phase of two stimuli presented simultaneously to achieve destructive interaction that minimizes the afferent modulation (balanced). Equivalent results were obtained using afferent responses to the stimuli applied independently.(ABSTRACT TRUNCATED AT 400 WORDS)