Discharge patterns of levator palpebrae superioris motoneurons during vertical lid and eye movements in the monkey.

1. We recorded single-unit activity in the caudal central nucleus (CCN) of the oculomotor complex in monkeys trained to make vertical saccadic, smooth-pursuit, and fixation eye movements. We confirmed that our recordings were from motoneurons innervating the upper lid, because small lesions placed at the sites of responsive units were recovered among neurons labeled by horseradish peroxidase (HRP) injections into the levator palpebrae superioris muscle. 2. For fixations above a threshold lid position, levator motoneurons discharged at a steady rate, which increased linearly with upward lid position. The average position sensitivity during fixation was 2.9 spikes/s per deg, and the average lid motoneuron was recruited into steady firing when the eye was looking 10 degrees down. 3. During upward saccades, levator motoneurons discharged a burst of spikes that began, on average, 7.3 ms before the lid movement if the saccade started from a straight-ahead position; the lead time decreased considerably as the initial eye and lid positions shifted downward. The firing rate usually reached its peak (130-280 spikes/s) at the very onset of the burst and declined gradually during the course of the saccade. The steady rate associated with the new fixation position was reached about halfway during the saccade. All units exhibited a pause in firing during the initial half of large downward saccades; during small saccades, the pause was inconspicuous or absent. 4. During vertical sinusoidal smooth pursuit, levator motoneurons exhibited a sinusoidal modulation in firing rate, which led eye position by an average of 23 degrees at 0.3 Hz. The average velocity sensitivity calculated from such data was 0.63 spikes/s per deg/s. 5. Although they exhibit a number of qualitative similarities, the discharge patterns of levator motoneurons and superior rectus motoneurons differ in several respects. First, during a blink, when the lid undergoes a large depression but the eye exhibits only a brief transient displacement, levator motoneurons cease firing completely, whereas superior rectus motoneurons continue to discharge. Second, for all types of coordinated lid and eye movements, levator motoneurons discharge at lower firing rates than do superior rectus motoneurons. Third, during saccades, levator motoneurons have less conspicuous and shorter-lasting bursts and pauses than do motoneurons involved in rotating the eye. 6. During upward gaze, the qualitative similarity of their burst-tonic discharge patterns suggests that levator and superior rectus motoneurons receive input signals that originate from a common source, but that the signals are processed differently to deal with the different loads facing these muscles.(ABSTRACT TRUNCATED AT 400 WORDS)

Brainstem afferents to the oculomotor omnipause neurons in monkey.

To determine how saccade-related areas in the brainstem address the saccade generator, we examined the afferents to the nucleus raphe interpositus. This region contains the omnipause neurons, which are pivotal in the generation of saccades. Horseradish peroxidase injected iontophoretically into the nucleus raphe interpositus retrogradely labeled a variety of brainstem nuclei. The greatest numbers of labeled neurons were in the paramedian pontomedullary reticular formation, in the nuclei reticularis gigantocellularis, and paragigantocellularis lateralis. Labeling was more modest but consistent in the interstitial nucleus of Cajal and the adjacent mesencephalic reticular formation, the middle gray of the superior colliculi, the region dorsolateral to the nucleus reticularis tegmenti pontis, and the medial vestibular nucleus. A few neurons were labeled around the habenulopeduncular tract and in the medial portion of the nucleus of the fields of Forel, in the nucleus reticularis medullaris ventralis, and in the spinal nucleus of the trigeminal nerve, the cochlear nucleus, and the superior olivary complex. The distribution and density of labeling suggest that omnipause neurons in the monkey are more intimately connected with other oculomotor structures than those in the cat. In addition, the rhombencephalic reticular afferents to the monkey omnipause neurons are more concentrated in their immediate vicinity than in the cat. The label consistently found dorsolateral to the nucleus reticularis tegmenti pontis may be a newly discovered link in saccade generation.

Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey.

1. With the use of single-unit recording, the reticular formation immediately caudal to the abducens nucleus was searched for saccadic burst neurons in alert, trained rhesus monkeys. We recorded 80 short- and long-lead burst neurons, investigated their connections, and quantitatively analyzed their discharge characteristics. 2. Like excitatory burst neurons located rostral to the abducens, these caudal burst neurons fire optimally for ipsilaterally directed saccades, fire less for vertical saccades, and fire minimally, if at all, for contralateral saccades. The direction associated with the maximum number of spikes was approximately along the horizontal axis (1 +/- 12 degrees (SD); n = 33). 3. The first spike of the burst led the saccade by 2-120 ms, depending on the unit. Neurons were divided into short lead (45%) and long lead (55%) using a burst-lead criterion of 15 ms. In the on-direction, the discharges of both types exhibited strong correlations between number of spikes in the burst and size of the horizontal saccade component; duration of the burst and duration of the saccade; and peak frequency of the burst and peak velocity of the saccade. These relations were looser for long-lead neurons than for short-lead neurons. 4. Horseradish peroxidase injected into the abducens nucleus retrogradely labeled cells in the contralateral reticular formation where burst neurons were recorded, showing that cells in this region make crossed monosynaptic connections. There was good agreement between the limits of this region, as determined physiologically and anatomically. 5. Microstimulation at the locus of recorded burst neurons elicited EMG potentials in the contralateral lateral rectus muscle of the appropriate sign and latency for a monosynaptic inhibitory projection to abducens motoneurons. Stimulation also elicited eye movements consistent with inhibition of the contralateral lateral rectus. 6. It is argued that these characteristics make it likely that the short-lead neurons are the source of the afference which generate the pause in contralateral abducens motoneuron firing during adducting saccades. These neurons are therefore analogous to the inhibitory burst neurons (IBNs) found in the cat. The characteristics of long-lead burst neurons, particularly their lead, make them less likely to subserve this function. These cells might be better suited to providing input to omnipause neurons or to the short-lead IBNs.

Basal interstitial nucleus of the cerebellum: cerebellar nucleus related to the flocculus.

We have shown that the monkey flocculus is not connected with any of the major, well-demarcated cerebellar nuclei. There is, however, a broadly distributed interstitial population of neurons in the white matter ventral to the cerebellar nuclei and extending into the peduncle of the flocculus; this population, previously undescribed in the monkey, has reciprocal connections with the flocculus (Langer et al., '85a,b). Several lines of evidence indicate that this collection of neurons, called the basal interstitial nucleus of the cerebellum (BIN/Cb), can justifiably be considered a nucleus. (1) Injection of horseradish peroxidase (HRP) into the flocculus always labels a group of neurons that lie immediately ventral to the well-demarcated cerebellar nuclei and extend posteromedially into the lateral margin of the nodulus and rostrolaterally around the caudal surface of the y-group, infiltrating the peduncle of the flocculus. (2) In Nissl-stained material there is a readily seen collection of neurons that are clearly distinct from the overlying cerebellar nuclei, with precisely the same distribution. These neurons have a characteristic morphology: they are intermediate-sized, chromatophilic, multipolar, and fusiform, and have rapidly tapering proximal dendrites. The cell nucleus is generally placed eccentrically in the cell body, against the plasma membrane or in one pole of the cell. The Nissl substance is usually finely granular in the center of the cell body and forms dense clumps adjacent to the cell membrane. (3) Anterograde label from injections of HRP or tritiated amino acids into the flocculus extends over the same group of neurons. In one brain with an HRP injection involving a part of the BIN/Cb there was a patchy, clustered distribution of labeled Purkinje cells extending throughout the flocculus and into the adjacent lateral parts of the simple lobule. The clusters were confined to the medial half of many of the floccular folia.

Brainstem afferents to the omnipause region in the cat: a horseradish peroxidase study.

"Omnipause" neurons (OPNs), located in the nucleus raphe pontis and the reticular formation, actively suppress saccadic eye movements during intersaccadic intervals. To determine the brainstem afferents that may inhibit the OPNs and thereby allow a saccade to occur, we injected horseradish peroxidase into the raphe pontis of four cats at the site of physiologically identified OPNs. Labeled neurons were found in a number of brainstem nuclei. The greatest concentrations, composed of small to medium-sized neurons, were located in a group of nuclei around the habenulopeduncular tract, in the rostral mesencephalic reticular formation, in the deep layers of the superior colliculus, and in parts of the subjacent cuneiform and subcuneiform reticular nuclei. Smaller numbers were found in the nucleus reticularis pontis oralis. Caudal to the injection site, labeled neurons were scattered in parts of the nuclei reticularis gigantocellularis, paragigantocellularis dorsalis, and paragigantocellularis lateralis. A few neurons were labeled in a restricted region of the causal part of the nucleus prepositus hypoglossi and in the nucleus reticularis medullaris ventralis. Larger numbers of neurons were labeled in the dorsal column nuclei and in parts of the cochlear nuclei. Smaller numbers were found in the spinal trigeminal nucleus, the lateral nucleus of the superior olive, and the fastigial nucleus of the cerebellum. The nonreticular brainstem projections may contribute sensory information in a number of modalities since OPNs respond to visual, somesthetic, and auditory stimuli. Our findings indicate a number of regions that may contain neural elements impinging on the OPNs. The best prospects for a saccade initiation signal from one of the labeled populations appear to be the meso-diencephalic reticular formation and/or the superior colliculus.

Efferent projections of the cat oculomotor reticular omnipause neuron region: an autoradiographic study.

Omnipause neurons (OPNs) are midline pontine neurons that are thought to be instrumental in the generation of saccadic eye movements. Inhibition of the tonically active OPNs is postulated to disinhibit the burst neurons that cause the saccadic discharge in motoneurons, leading to a saccade. To test whether the anatomical connections of OPNs are consistent with this scheme, we studied the efferent projections of the OPN region by using the technique of anterograde transport of tritiated amino acids. Injections into the OPN region yield a distinct pattern of labeled tracts and terminal fields that is different from the patterns following control injections in the surrounding reticular formation. Caudally, there are terminal fields over the paramedian reticular formation, the caudal part of the medial accessory nucleus of the inferior olivary complex, the nucleus prepositus hypoglossi, and the nucleus reticularis paragigantocellularis dorsalis caudal and ventromedial to the abducens nuclei. Rostrally, terminal label is distributed over parts of the nuclei reticularis pontis caudalis and oralis, the nucleus raphe pontis, the nucleus reticularis tegmenti pontis, the mesencephalic reticular nucleus, the central gray, and the nucleus of the H-field. Thus, there are direct projections from the OPN region to all areas known to contain burst neurons. In addition, OPNs also apparently have indirect access to the spinal cord and cerebellum. Many of the latter connections parallel the efferent projections of the superior colliculus.