Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. II. Correlation with output pathways of secondary neurons

Abstract

1. Intracellular recordings were made from secondary neurons in the vestibular nuclei of barbiturate-anesthetized squirrel monkeys. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by stimulation of the ipsilateral vestibular nerve (Vi) were measured. An electrophysiological paradigm, described in the preceding paper (26), was used to determine the proportion of irregularly (I) and regularly (R) discharging Vi afferents making direct connections with individual secondary neurons. The results were expressed as a % I index, an estimate for each neuron of the percentage of the total Vi monosynaptic input that was derived from I afferents. The secondary neurons were also classified as I, R, or M cells, depending on whether they received their direct Vi inputs predominantly from I or R afferents or else from a mixture (M) of both kinds of Vi fibers. The neurons were located in the superior vestibular nucleus (SVN) or in the rostral parts of the medical or lateral (LVN) vestibular nuclei. 2. Antidromic activation or reconstruction of axonal trajectories after intrasomatic injection of horseradish peroxidase (HRP) was used to identify three classes of secondary neurons in terms of their output pathways: 1) cerebellar-projecting (Fl) cells innervating the flocculus (n = 26); 2) rostrally projecting (Oc) cells whose axons ascended toward the oculomotor (IIIrd) nucleus (n = 27); and 3) caudally projecting (Sp) cells with axons descending toward the spinal cord (n = 13). Two additional neurons, out of 21 tested, could be antidromically activated both from the level of the IIIrd nucleus and from the spinal cord. 3. The Vi inputs to the various classes of relay neurons differed. As a class, Oc neurons received the most regular inputs. Sp neurons had more irregular inputs. Fl neurons were heterogeneous with similar numbers of R, M, and I neurons. The mean values (+/- SD) of the % I index for the Oc, Fl, and Sp neurons were 34.7 +/- 24.7, 51.9 +/- 30.4, and 61.8 +/- 18.0%, respectively. Only the Oc neurons had a % I index that was similar to the proportion of I afferents (34%) in the vestibular nerve (cf. Ref. 26). 4. The commissural inputs from the contralateral vestibular nerve (Vc) also differed for the three projection classes. Commissural inhibition was most common in Fl cells: 22/25 (88%) of the neurons had Vc inhibitory postsynaptic potentials (IPSPs) and 1/25 (4%) had a Vc EPSP. In contrast, Vc inputs were only observed in approximately half the Oc and Sp neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys

“…Goldberg et al (1987) showed that 75% of secondary vestibular neurons in the vestibular nucleus receive monosynaptic inputs from afferents with a broad range ofresponse properties. Highstein et al (1987) subdivided the population of secondary neurons according to their projection sites and found that 57% of identified interneurons in the VOR pathways received monosynaptic inputs from afferents with a broad range of response properties. However, Highstein et al (1987) interpreted the wide range of vestibular inputs to VOR interneurons as contamination of their sample with other "pause-burst" neurons and concluded that VOR pathways receive input mainly from afferents with regular spontaneous discharge.…”

“…Highstein et al (1987) subdivided the population of secondary neurons according to their projection sites and found that 57% of identified interneurons in the VOR pathways received monosynaptic inputs from afferents with a broad range of response properties. However, Highstein et al (1987) interpreted the wide range of vestibular inputs to VOR interneurons as contamination of their sample with other "pause-burst" neurons and concluded that VOR pathways receive input mainly from afferents with regular spontaneous discharge. Our data disagree with the interpretation and Lisberger * Vestibular Inputs for the VOR of Highstein et al (1987) but agree with their data as well as in the gain of the VOR than are the eye movements evoked by with those of Goldberg et al (1987).…”

“…However, Highstein et al (1987) interpreted the wide range of vestibular inputs to VOR interneurons as contamination of their sample with other "pause-burst" neurons and concluded that VOR pathways receive input mainly from afferents with regular spontaneous discharge. Our data disagree with the interpretation and Lisberger * Vestibular Inputs for the VOR of Highstein et al (1987) but agree with their data as well as in the gain of the VOR than are the eye movements evoked by with those of Goldberg et al (1987). At least for the VOR single electrical pulses present results).…”

“…Comparisons of the responses to head rotations of primary afferents (Goldberg and Fernandez,197 la) and of neurons that receive monosynaptic inputs from the primary afferents Shimazu and Precht, 1965;Melvill Jones and Milsum,, 1970;Shinoda and Yoshida, 1974) have demonstrated similar bimodal distributions of the time constants of their responses to steps of head acceleration. Comparisons of the responses of the same groups of primary and secondary neurons to electrical stimulation of the vestibular apparatus Highstein et al, 1987) have established correlations between the thresholds of central vestibular neurons and of vestibular afferents with different physiological properties. These authors found that interneurons in the disynaptic VOR pathways to the oculomotor nuclei received less input from afferents with irregular spontaneous firing than did interneurons in pathways to the spinal cord.…”

Galvanic stimulation of the vestibular periphery in guinea pigs during passive whole body rotation and self-generated head movement

“…On the basis of these results, they concluded that irregular otolith afferents might be essential for the generation of steady-state nystagmus during off-vertical axis rotations (OVAR) and for velocity storage and the VOR at sinusoidal frequencies Ͻ0.1 Hz. The limited effects of irregular afferent "functional" ablation are surprising, as experimenters have also shown that there is no preferential innervation of second-order vestibular neurons by the different afferent types (Boyle et al 1992;Chen-Huang et al 1997;Highstein et al 1987). One possible explanation for this apparent paradox is the influence of extravestibular factors such as target distance or attention (Chen-Huang et al 1997;Chen-Huang and McCrea 1998) on the responses of neurons within the vestibular nucleus.…”