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Direct projections from the superior colliculus (SC) to the paramedian pontine reticular formation (PPRF) have been demonstrated anatomically. The PPRF contains cells called excitatory burst neurons (EBNs) that execute the final premotoneuronal processing for saccadic eye movements, as well as other burst cells called long-lead burst neurons (LLBNs). Previous electrophysiological tests in monkey have failed to find evidence for monosynaptic connections from the SC to EBNs, but have shown that direct projections to LLBNs exist. The validity of these results has been questioned because EBNs are known to be inhibited during periods of fixation by cells called omnipause neurons (OPNs). In later experiments in cat, the stimulus in the SC was triggered during saccades (when OPNs are off) and direct connections to EBNs were found. The present experiments were conducted to determine whether direct connections from the SC to EBNs could be demonstrated in monkey. LLBNs located near EBNs were also recorded. Single-pulse stimuli were delivered at sites in the SC at current levels well above those required to evoke saccades with pulse train stimuli. The stimuli were triggered shortly after the onset of ipsilateral or contralateral saccades and also slightly after the end of saccades. A sample of 21 EBNs was recorded and none were activated by postsaccadic stimulation or during contralateral saccades. The high spontaneous discharge rates of EBNs during ipsilateral saccades made activation of these cells more difficult to detect; however, when the results were quantified by peristimulus time histograms aligned on stimulus onset, only 1/21 EBNs showed evidence of activation in the monosynaptic range of latencies (<1.6 ms), 13 EBNs were activated at di- or polysynaptic latencies, and 7 were not activated. In contrast, 15/21 LLBNs were activated with latencies in the monosynaptic range. Further evidence supporting the absence of direct connections to EBNs was obtained by realigning the peristimulus time histograms for a subset of EBNs with similar firing rates on the time of occurrence of the last spike before stimulus onset. A subset of EBNs was also studied during drowsy ipsilaterally directed eye drifts, during which these cells were firing at low spontaneous rates and OPNs were off. No evidence for direct connections to EBNs was found in this behavioral state. The variance in results obtained for cat and monkey may be due to a species difference that reflects the more complex signal processing required in the monkey's saccadic system.

1. In this study we sought to characterize the visual motion processing that exists in the dorsolateral pontine nucleus (DLPN) and make a comparison with the reported visual responses of the middle temporal (MT) and medial superior temporal (MST) areas of the monkey cerebral cortex. The DLPN is implicated as a component of the visuomotor interface involved with the regulation of smooth-pursuit eye movements, because it is a major terminus for afferents from MT and MST and also the source of efferents to cerebellar regions involved with eye-movement control. 2. Some DLPN cells were preferentially responsive to discrete (spot and bar) visual stimuli, or to large-field, random-dot pattern motion, or to both discrete and large-field visual motion. The results suggest differential input from localized regions of MT and MST. 3. The visual-motion responses of DLPN neurons were direction selective for 86% of the discrete visual responses and 95% of the large-field responses. Direction tuning bandwidths (full-width at 50% maximum response amplitude) averaged 107 degrees and 120 degrees for discrete and large-field visual motion responses, respectively. For the two visual response types, the direction index averaged 0.95 and 1.02, indicating that responses to stimuli moving in preferred directions were, on average, 20 and 50 times greater than responses to discrete or large-field stimulus movement in the opposite directions, respectively. 4. Most of the DLPN visual responses to movements of discrete visual stimuli exhibited increases in amplitude up to preferred retinal image speeds between 20 and 80 degrees/s, with an average preferred speed of 39 degrees/s. At higher speeds, the response amplitude of most units decreased, although a few units exhibited a broad saturation in response amplitude that was maintained up to at least 150 degrees/s before the response decreased. Over the range of speeds up to the preferred speeds, the sensitivity of DLPN neurons to discrete stimulus-related, retinal-image speed averaged 3.0 spikes/s per deg/s. The responses to large-field visual motion were less sensitive to retinal image speed and exhibited an average sensitivity of 1.4 spikes/s per deg/s before the visual response saturated. 5. DLPN and MT were quantitatively comparable with respect to degree of direction selectivity, retinal image speed tuning, and distribution of preferred speeds. Many DLPN receptive fields contained the fovea and were larger than those of MT and more like MST receptive fields in size.(ABSTRACT TRUNCATED AT 400 WORDS)

1. Anatomical and single-unit recording studies suggest that the dorsolateral pontine nucleus (DLPN) in monkey is a major link in the projection of descending visual motion information to the cerebellum. Such studies coupled with cortical and cerebellar lesion results suggest a major role for this basilar pontine region in the mediation of smooth-pursuit eye movements. 2. To provide more direct evidence that this pontine region is involved in the control of smooth-pursuit eye movements, focal chemical lesions were made in DLPN in the vicinity of previously recorded visual motion and pursuit-related neurons. Eye movement responses were subsequently recorded in these lesioned animals under several behavioral paradigms. 3. A major deficit in smooth-pursuit performance was produced after unilateral DLPN lesions generated either reversibly with lidocaine or more permanently with ibotenic acid. Pursuit impairments were observed during steady-state tracking of sinusoidal target motion as well as during the initiation of pursuit tracking to sudden ramp target motion. Through the use of the latter technique, initial eye acceleration was reduced to less than one-half of normal for animals with large lesions of the dorsolateral and lateral pontine nuclei. 4. The pursuit deficit in all animals was directional in nature and was not dependent on the visual hemifield in which the motion stimulus occurred. The largest effect for horizontal tracking occurred in all animals for pursuit directed ipsilateral to the lesion. Animals also showed major deficits in one or both directions of vertical pursuit, although the primary direction of the vertical impairment was variable from animal to animal. 5. Chemical lesions in the DLPN also produced comparable deficits in the initiation of optokinetic-induced smooth eye movements in the ipsilateral direction. In contrast to this effect on the initial optokinetic response, in the one lesioned animal studied during prolonged constant velocity optokinetic drum rotation, smooth eye speed increased slowly over a 10- to 15-s period to reach a level that closely matched drum speed. These results suggest that pathways outside the DLPN can generate the steady-state optokinetic response. 6. Saccades to stationary targets were normal after DLPN lesions, but corrective saccades made to targets moving in the direction ipsilateral to the lesion were much more hypometric than similar prelesion control saccades. 7. The pursuit deficits produced by lidocaine injections recovered within 30 min. The ibotenic acid deficits were maximal approximately 1 day after the injection and recovered rapidly thereafter over a time period of 3-7 days.(ABSTRACT TRUNCATED AT 400 WORDS)

A small region in the dorsal midline portion of the nucleus reticularis tegmenti pontis (NRTP) in monkeys contains neurons that respond to focal visual stimuli or during saccadic eye movements or both. None of these cells or any others in this region respond to the motion of large visual fields (optokinetic stimulation), although such responses were specifically sought. Thus, this group of NRTP neurons forms a completely different set of cells than those previously described in more rostral but closely adjacent portions of the pontine nuclei which respond well to optokinetic stimulation. The most frequently encountered cell type in this region of NRTP (153 neurons) produced a high-frequency burst of discharges during saccadic eye movements. Neural discharge (burst intensity or duration) was not related to saccade metrics. Instead, peak burst frequency and/or the number of spikes in a unit's burst reached a maximum when the saccade moved the eyes to a circumscribed region (movement field) of the animal's visual field. There were two subtypes of these burst neurons. In one type (44%) the movement fields were smaller and entirely contained within the oculomotor range. In the other type (56%) the movement fields consisted of a whole sector (some as wide as 180 degrees) of the entire oculomotor range. All the neurons in this sample that we were able to test in total darkness continued to produce bursts of discharges of similar profile during spontaneous saccades into their movement field. All the movement fields were retinotopically organized, although a few cells (22%) showed a marked variation of burst metrics with initial eye position. Another small group of cells in NRTP (8 neurons) responded to small spots of light turned on within a circumscribed region of the visual field while the animal maintained fixation on a separate spot of light. These visual neurons produced no saccade-related discharge. A larger group of neurons (24 out of 52 tested cells) produced both a visual response and a saccadic burst. The visual field of this type of cell was always smaller and was contained within the movement field of the cell. The response of both types of NRTP visual neurons was enhanced when the visual stimulus was to be the target for a saccadic eye movement. On double-saccade trials the visual stimulus was never present in the hemifield containing the cell's visual field.(ABSTRACT TRUNCATED AT 400 WORDS)