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Notes: Summary Vestibulocollic (VCR) and vestibulo-ocular (VOR) reflexes were studied during angular rotation in the horizontal plane in precollicular decerebrate cats. Angular position was modulated by sinusoids or sums of sinusoids with frequencies ranging from 0.05 to 5 Hz. Reflex motor output was measured by recording electromyographic (EMG) activity of the lateral rectus and dorsal neck muscles and discharge of abducens motoneurons. Measured with respect to input angular acceleration VCR motor output displayed a second order lag at low frequencies, bringing mean EMG phase (−136 °) and gain slope (−35 dB/ decade) close to those of an angular position signal at 0.2 Hz. At higher frequencies the lag was counteracted by a second order lead bringing mean phase (−52 °) and gain slope (−5.6 dB/decade) back close to those of an angular acceleration signal at 3 Hz. By contrast, mean phase (−113 ° to −105 °) and gain slope (−21 to −28 dB/decade) of the VOR motor output remained close to those of an angular velocity signal across the entire frequency range. The data suggest that neural pathways producing the VCR receive selective input from “irregular type” horizontal semicircular canal afferents which provide one lag and one lead in the overall transfer function while the other lag and lead are produced by central pathways. Transaction of the medial longitudinal fasciculus (MLF), which eliminates all of the most direct (three neuron) arcs of the horizontal VCR, did not cause any detectable change in the horizontal VCR at either low or high frequencies. Reductions in overall gain occurred in some cases but these could be attributed to damage to axons outside the MLF. Less direct pathways, probably including vestibulo-reticulospinal pathways, are thus able to produce both the low-frequency, phase-lagging and high-frequency, phase-leading components of the horizontal VCR.

Notes: Summary We studied the influence of static head position on the horizontal nystagmus produced by caloric, rotational and optokinetic stimulation in alert squirrel monkeys. Caloric nystagmus is stronger for nose up (NU) than for nose down (ND) pitches; so, for example, slow-phase eye velocity is four times larger in supine than in prone positions. A similarly directed asymmetry occurs in the horizontal vestibulo-ocular (HVOR) responses to longduration, constant angular-head accelerations, but not to midband (0.1 Hz) sinusoidal head rotations. Consistent with a first-order model of the HVOR, the low-frequency or acceleration gain of the reflex (GA) is equal to the product of the midband velocity gain (GV) and a time constant (TVOR). GV is proportional to the cosine of the angle between the horizontal-canal plane and the plane of rotation, from which it is concluded that signals from the horizontal, but not from the vertical canals contribute to the HVOR. TVOR can be as much as twice as large in NU than in ND positions. GA is proportional to TVOR and it, too, shows a NU-ND asymmetry. The time constant of optokinetic afternystagmus (TOKAN) was also studied. Since TVOR and TOKAN are modified in similar ways by static tilts, it is concluded that head position affects the time constants by way of velocity-storage mechanisms. Evidence is presented that the position-dependent modification of velocity storage is otolith-mediated. The results are used to analyze the mechanisms of caloric nystagmus. The caloric response consists of a convective component (CC), as originally envisioned by Bárány (1906), and a nonconvective component (NC). CC accounts for 75% of the caloric response in the conventional supine testing position. Both components can be affected by the position-dependent modification of TVOR or, equivalently, of GA. It has been suggested that two mechanisms might contribute to NC: 1) a direct thermal effect on hair cells or afferents; or 2) a thermal expansion of labyrinthine fluids that results in a cupular displacement. Both theoretical and experimental evidence indicates that only the first of these mechanisms could result in the steady-state caloric response that is observed in the absence of convection (e.g., in spaceflight and after canal plugging) and that contributes to the prone-supine asymmetry seen in caloric testing.

Notes: Summary Recordings were made from secondary vestibular axons in the medial longitudinal fasciculus (MLF) of barbiturate-anesthetized squirrel monkeys. Antidromic stimulation techniques were used to identify the axons as belonging to one of three classes of neurons: vestibulo-oculo-collic (VOC) neurons project both to the extraocular motor nuclei and to the spinal cord; vestibulo-ocular (VO) neurons do not have a spinal projection; and vestibulocollic (VC) neurons do not have an oculomotor projection. Galvanic stimulation was used to show that axons of all three classes received excitatory inputs from one labyrinth and inhibitory inputs from the other. VOC axons were confined to the MLF contralateral to the labyrinth from which they were excited. They made up more than half of the vestibular axons descending in the contralateral medial vestibulospinal tract (MVST), but less than one-quarter of those ascending in the contralateral MLF to the level of the oculomotor nucleus. Spinal projections were restricted to cervical segments with about half of the axons reaching segment C6. Conduction velocities, measured for Co-projecting axons, were similar for VOC and VC axons and were typically 25–50 m/s. Unlike the situation in the rabbit (Akaike et al. 1973) and cat (Akaike 1983), none of the MVST axons had conduction velocities 〉 75 m/s. The morphology of VOC neurons was studied by injection of horseradish peroxidase (HRP) into 60 physiologically identified axons in the MLF. Since individual axons were only stained for short distances, it was not possible to ascertain their complete branching patterns. Labeled fibers could be traced to an origin in and around the ventral lateral vestibular nucleus. This localization was confirmed by comparing the distributions within the vestibular nuclei of neurons retrogradely labeled from the upper cervical spinal cord (this study) and from the oculomotor nucleus (McCrea et al. 1987a; Highstein and McCrea 1988). VOC axons reached the contralateral MLF at the level of the abducens nucleus and immediately divided into an ascending and a descending, usually thicker, branch. Seven VOC axons could be traced to the extraocular motor nuclei; three terminated in the medial aspect of the oculomotor nucleus bilaterally and four terminated in the medial aspect of the contralateral abducens nucleus. The former axons may be part of a crossed, excitatory anterior-canal pathway; the latter, part of a similar horizontal-canal pathway. There were no terminations in the trochlear nucleus even though 12 labeled fibers passed close to it. VOC axons projected to several brainstem nuclei, including the contralateral interstitial nucleus of Cajal, cell groups in the region of the medial longitudinal fasciculus rostral to the abducens nucleus, the nucleus prepositus, the nucleus raphe obscuris, Roller's nucleus, and the paramedian medullary reticular formation. Virtually all of the above connections, except for the bilateral projection to the oculomotor nucleus, were contralateral to the cells of origin. The results in the squirrel monkey are compared with previous studies of VOC neurons in the cat (Isu and Yokota 1983; Uchino and Hirai 1984; Isu et al. 1988). In both species, VOC neurons make up a large proportion of contralaterally projecting MVST fibers. On the other hand, such dual-projecting neurons may provide a considerably smaller fraction of the secondary vestibular axons reaching the oculomotor nucleus in the monkey than they do in the cat.

Notes: Summary The eye movements produced by constant-speed rotations about an earth-horizontal axis (EHA) are similar in the alert squirrel monkey to those observed in other species. During EHA rotations, there are persistent eye movements, including a nonreversing nystagmus at lower rotation speeds and either a direction-reversing nystagmus or sinusoidal eye movements at higher rotation speeds. Horizontal eye movements are produced by “barbecuespit” (yaw) rotations, vertical eye movements by “head-over-heels” (pitch) rotations. The responses can be viewed as composed of a bias component, reflected in the nonreversing nature of the nystagmus, and a cyclic component, reflected in the periodic modulation of slow-phase eye velocity as head position varies. Vestibular-nerve recordings in the barbiturate-anesthetized monkey indicate that neither semicircular-canal nor otolith afferents give rise to a directionally specific dc signal which can account for the bias component. Apparently the appropriate dc signal has to be constructed centrally from a sinusoidal or ac peripheral input. The otolith organs are a likely source of this peripheral input, although contributions from the semicircular canals and from somatosensory receptors must also be considered. Our results suggest that the directional information required to distinguish rotation direction, rather than being contained in the discharge of individual otolith afferents, is encoded across a population of afferents. Possible sources of such information are the phase differences in the sinusoidal responses of otolith afferents differing in their functional polarization vectors.