Jay M. Goldberg

Responses of Squirrel Monkey Vestibular Neurons to Audio-Frequency Sound and Head Vibration

A study was made of the response of peripheral vestibular neurons in the squirrel monkey to head vibration and air-borne sound in the frequency range from 50-4 00 Hz. Responses were measured in terms of the phase locking of discharge and changes in firing rate. The lowest phase-locking thresholds for vibration were -70 to -80 dB re 1 g, and median values in the most sensitive frequency range (200-400 Hz) were -20 to -40 dB re 1 g; the minimum and median thresholds for sound were 76 and 120-130 dB SPL, respectively. Rate-change thresholds were 10-30 dB above phase-locking thresholds. The squirrel monkey sacculus has no special sensitivity to vibration in comparison with the other vestibular end-organs; the median phase-locking threshold to sound of saccular neurons exceeded 100 dB SPL. Irregularly discharging neurons are more sensitive than regularly discharging units. Evidence is presented that the response to intense sound involves a hair-cell mechanism.

Afferent diversity and the organization of central vestibular pathways

Abstract This review considers whether the vestibular system includes separate populations of sensory axons innervating individual organs and giving rise to distinct central pathways. There is a variability in the discharge properties of afferents supplying each organ. Discharge regularity provides a marker for this diversity since fibers which differ in this way also differ in many other properties. Postspike recovery of excitability determines the discharge regularity of an afferent and its sensitivity to depolarizing inputs. Sensitivity is small in regularly discharging afferents and large in irregularly discharging afferents. The enhanced sensitivity of irregular fibers explains their larger responses to sensory inputs, to efferent activation, and to externally applied galvanic currents, but not their distinctive response dynamics. Morphophysiological studies show that regular and irregular afferents innervate overlapping regions of the vestibular nuclei. Intracellular recordings of EPSPs reveal that some secondary vestibular neurons receive a restricted input from regular or irregular afferents, but that most such neurons receive a mixed input from both kinds of afferents. Anodal currents delivered to the labyrinth can result in a selective and reversible silencing of irregular afferents. Such a functional ablation can provide estimates of the relative contributions of regular and irregular inputs to a central neuron’s discharge. From such estimates it is concluded that secondary neurons need not resemble their afferent inputs in discharge regularity or response dynamics. Several suggestions are made as to the potentially distinctive contributions made by regular and irregular afferents: (1) Reflecting their response dynamics, regular and irregular afferents could compensate for differences in the dynamic loads of various reflexes or of individual reflexes in different parts of their frequency range; (2) The gating of irregular inputs to secondary VOR neurons could modify the operation of reflexes under varying behavioral circumstances; (3) Two-dimensional sensitivity can arise from the convergence onto secondary neurons of otolith inputs differing in their directional properties and response dynamics; (4) Calyx afferents have relatively low gains when compared with irregular dimorphic afferents. This could serve to expand the stimulus range over which the response of calyx afferents remains linear, while at the same time preserving the other features peculiar to irregular afferents. Among those features are phasic response dynamics and large responses to efferent activation; (5) Because of the convergence of several afferents onto each secondary neuron, information transmission to the latter depends on the gain of individual afferents, but not on their discharge regularity.

A regional ultrastructural analysis of the cellular and synaptic architecture in the chinchilla cristae ampullares

The chinchilla crista ampullaris was studied in 10 samples, each containing 32 consecutive ultrathin sections of the entire neuroepithelium. Dissector methods were used to estimate the incidence of various synaptic features, and results were confirmed in completely reconstructed hair cells. There are large regional variations in cellular and synaptic architecture. Type I and type II hair cells are shorter, broader, and less densely packed in the central zone than in the intermediate and peripheral zones. Complex calyx endings are most common centrally. On average, there are 15–20 ribbon synapses and 25–30 calyceal invaginations in each type I hair cell. Synapses and invaginations are most numerous centrally. Central type II hair cells receive considerably fewer afferent boutons than do peripheral type II hair cells, but have similar numbers of ribbon synapses. The numbers are similar because central type II hair cells make more synapses with the outer faces of calyx endings and with individual afferent boutons. Most afferent boutons get one ribbon synapse. Boutons without ribbon synapses were only found peripherally, and boutons getting multiple synapses were most frequent centrally. Throughout the neuroepithelium, there is an average of three to four efferent boutons on each type II hair cell and calyx ending. Reciprocal synapses are rare. Most synaptic ribbons in type I hair cells are spherules; those in type II hair cells can be spherical or elongated and are particularly heterogeneous centrally. Consistent with the proposal that the crista is concentrically organized, the intermediate and peripheral zones are each similar in their cellular and synaptic architecture near the base and near the planum. An especially differentiated subzone may exist in the middle of the central zone. J. Comp. Neurol. 389:419–443, 1997.

Discharge charateristics of neurons in anteroventral and dorsal cochlear nuclei of cat

Abstract A comparison was made of the discharge characteristics in two regions of the cochlear nuclear complex, the dorsal nucleus (DCN) and the spherical cell region (SCR) of the anteroventral nucleus. SCR neurons have narrow excitatory tuning curves and usually do not have inhibitory sidebands. The response to tone-burst stimulation is primary-like. Rate-intensity functions are almost always monotonic. The spacing of action potentials is irregular. Discharge may be phase-locked for frequencies exceeding 3 kHz. DCN neurons have more complicated discharge characteristics. Excitatory tuning curves may be broad or narrow and, in some cases, are multipeaked. Inhibitory sidebands are common and are especially prominent in units with narrow tuning curves. The response to tone bursts may be simple or complex. Complex response patterns involve silent pauses in discharge or the gradual buildup of activity. On occasion afterdischarges are seen. Many neurons, particularly those with complex response patterns, exhibit non-monotonic rate-intensity functions. Steady-state discharge patterns are regular. Phase-locking is usually limited to frequencies below 1.5 kHz. Results are discussed in terms of the morphology of the DCN and SCR.

Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents

Vestibular-nerve afferents classified as regularly or irregularly discharging also differ in their response dynamicsa, 4,13,14, in their sensitivites to natural stimulationa,4,14 and to electrical stimulation of efferent pathways 6, and in their conduction velocitiesS, 14. The cellular mechanisms determining the differences in discharge properties of the afferents are only poorly understood. In the present study, galvanic currents were used to define possible stages of the transduction process at which differences in response dynamics and discharge regularity may arise. Evidence will be presented that externally applied currents bypass earlier, mechanical stages and that tb_ey may actually influence discharge by acting near the postsynaptic trigger site the place in the afferent axon where impulses normally arise. Data were obtained from 16 barbiturate-anesthe tized adult male squirrel monkeys (Saimiri seiureus). Surgical and recording procedures have been described previously, as have the methods for natural stimulation and for identifying the end organ innervated by any afferent 2. Regularity of discharge was quantified by a normalized coefficient of variation (cv*), appropriate to a mean interval of 15 m s ! Units were classified as regular (cv* < 0.10), intermediate (0.10 _< cv* < 0.30) or irregular (cv* > 0.30). Electric currents were delivered between two chiorided silver wires (0.25 mm diameter), which were insulated to within 1 mm of their tips. One electrode was snugly fit into the perilymphatic space of the vestibule through a small hole made in the bony promontory; the other electrode was lodged in the hypotympanic space of the middle ear. Galvanic stimuli are called cathodal (-) or anodal (+) , in conformity with the polarity of the perilymphatic electrode. Cathodal currents were invariably found to increase afferent discharge, whereas anodal currents always decreased it. Sinusoidal head rotations and sinusoidal galvanic currents both led to responses with low harmonic distortion (near 5 ~o). Gains and phases extracted by Fourier analysis and expressed relative to peak head velocities or to peak currents were not systematically affected by stimulus magnitude. Results for 9 semicircular-canal units are summarized in Bode plots (Fig. 1). Responses to natural stimulation (Fig. 1A, C) are similar to those described previously1 and include two effects not seen in

Projections of the inferior colliculus in the monkey.

Abstract The projections of the inferior colliculus were studied in the rhesus monkey. The major component of these projections ascends in the brachium of the inferior colliculus. The fibers of the inferior brachium originate from the inferior colliculus on both sides and distribute in the midbrain to the parabrachial region of the lateral tegmentum and to the interstitial nucleus of the inferior brachium. Within the medial geniculate nucleus brachium fibers terminate in the rostral part of the principal division and in the magnocellular division. No fibers end in the caudal part of the principal division or in the posterior nucleus. Fibers arising from the inferior colliculus also terminate in the contralateral inferior colliculus, in the periaqueductal gray and in the deep layers of the superior colliculus. Descending projections from the inferior colliculus enter the tectopontine tract and the lateral lemniscus. The tectopontine tract appears to end in the lateral pontine nuclei. Fibers descending in the lateral lemniscus terminate primarily in the medial preolivary nucleus but there are additional endings in the ventral nucleus of the lateral lemniscus, the lateral preolivary nucleus and the retro-olivary region.

Influence of static head position on the horizontal nystagmus evoked by caloric, rotational and optokinetic stimulation in the squirrel monkey

SummaryWe 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.

Contributions of regularly and irregularly discharging vestibular-nerve inputs to the discharge of central vestibular neurons in the alert squirrel monkey

Abstract The discharge of neurons in the vestibular nuclei was recorded in alert squirrel monkeys while they were being sinusoidally rotated at 2 Hz. Type I position-vestibular-pause (PVP I) and vestibular-only (V I) neurons, as well as a smaller number of other type I and type II eye-plus-vestibular neurons were studied. Many of the neurons were monosynaptically related to the ipsilateral vestibular nerve. Eye-position and vestibular components of the rotation response were separated by multiple regression. Anodal currents, simultaneously delivered to both ears, were used to eliminate the head-rotation signals of irregularly discharging (I) vestibular-nerve afferents, presumably without affecting the corresponding signals of regularly discharging (R) afferents. R and I inputs to individual central neurons were determined by comparing rotation responses with and without the anodal currents. The bilateral currents, while reducing the background discharge of all types of neurons, did not affect the mean vestibular gain or phase calculated from a population of PVP I neurons or from a mixed population consisting of all type I units. From this result, it is concluded that I inputs are canceled at the level of secondary neurons. The cancellation may explain why the ablating currents do not affect the gain and phase of the vestibulo-ocular reflex. While cancellation was nearly perfect on a population basis, it was less so in individual neurons. For some neurons, the ablating currents decreased vestibular gain, while for other neurons the vestibular gain was increased. The former neurons are interpreted as receiving a net excitatory (I-EXC) I input, the latter neurons, a net inhibitory (I-INH) input. When compared with the corresponding R inputs, the I inputs were usually small and phase advanced. Phase advances were larger for I-EXC than for I-INH inputs. The sign and magnitude of the I inputs were unrelated to other discharge properties of individual neurons, including discharge regularity and the phase of vestibular responses measured in the absence of the ablating currents. Unilateral currents were used to assess the efficacy of ipsilateral and contralateral pathways. Ipsilateral pathways were responsible for almost all of the effects seen with bilateral currents. The results suggest that the vestibular signals carried by central neurons, even by those neurons receiving a monosynaptic vestibular-nerve input, are modified by polysynaptic pathways.

Morphophysiological and ultrastructural studies in the mammalian cristae ampullares

There are three kinds of afferent terminations in the cristae ampullares. Calyx units innervate a few neighboring type I hair cells. Bouton units contact several type II hair cells. Dimorphic units innervate both kinds of receptors. Axon diameters are largest for calyx fibers and smallest for bouton fibers. Dimorphic units supply all parts of the sensory epithelium. Calyx units are confined to the central zone of the crista and bouton units to its peripheral zone. Intra-axonal labeling was used to determine the innervation patterns of physiologically characterized afferents. Calyx units are irregularly discharging. Dimorphic units in the central zone have a more irregular discharge than those in the peripheral zone. Bouton units, which have also been identified by their slow conduction velocities, are regularly discharging. An afferents discharge regularity, sensitivity to externally applied galvanic currents and response dynamics are more closely related to its epithelial location than to its branching pattern or to the types and number of hair cells it contacts. Of the various discharge properties studied, only the rotational gains seemed closely related to terminal morphology. Afferents innervating the central and peripheral zones differ in their innervation patterns and discharge properties. A preliminary ultrastructural study indicates that there also are regional variations in synaptic organization. Type II hair cells in the peripheral zone are contacted by many more afferent boutons than those in the central zone. Individual central boutons have multiple ribbon synapses with type II hair cells, whereas each peripheral bouton usually has a single synaptic contact. Synapses between type II hair cells and calyx endings are common centrally, but not peripherally. Two synaptic features did not vary regionally: 1) type I hair cells usually make 10-20 ribbon synapses with their calyx endings; and 2) each type II hair cell is contacted by 2-6 efferent endings. The number of efferent boutons in contact with each calyx ending declines slightly from the peripheral zone to the central zone. Reciprocal synapses were rare.

Dual projections of secondary vestibular axons in the medial longitudinal fasciculus to extraocular motor nuclei and the spinal cord of the squirrel monkey

SummaryRecordings 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, Rollers 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.