Second-order vestibular neurons form separate populations with different membrane and discharge properties.

Membrane and discharge properties were determined in second-order vestibular neurons (2 degrees VN) in the isolated brain of grass frogs. 2 degrees VN were identified by monosynaptic excitatory postsynaptic potentials after separate electrical stimulation of the utricular nerve, the lagenar nerve, or individual semicircular canal nerves. 2 degrees VN were classified as vestibulo-ocular or -spinal neurons by the presence of antidromic spikes evoked by electrical stimulation of the spinal cord or the oculomotor nuclei. Differences in passive membrane properties, spike shape, and discharge pattern in response to current steps and ramp-like currents allowed a differentiation of frog 2 degrees VN into two separate, nonoverlapping types of vestibular neurons. A larger subgroup of 2 degrees VN (78%) was characterized by brief, high-frequency bursts of up to five spikes and the absence of a subsequent continuous discharge in response to positive current steps. In contrast, the smaller subgroup of 2 degrees VN (22%) exhibited a continuous discharge with moderate adaptation in response to positive current steps. The differences in the evoked spike discharge pattern were paralleled by differences in passive membrane properties and spike shapes. Despite these differences in membrane properties, both types, i.e., phasic and tonic 2 degrees VN, occupied similar anatomical locations and displayed similar afferent and efferent connectivities. Differences in response dynamics of the two types of 2 degrees VN match those of their pre- and postsynaptic neurons. The existence of distinct populations of 2 degrees VN that differ in response dynamics but not in the spatial organization of their afferent inputs and efferent connectivity to motor targets suggests that frog 2 degrees VN form one part of parallel vestibulomotor pathways.

Principles of linear and angular vestibuloocular reflex organization in the frog.

We compared the spatial organization patterns of linear and angular vestibuloocular reflexes in frogs by recording the multiunit spike activity from cranial nerve branches innervating the lateral rectus, the inferior rectus, or the inferior obliquus eye muscles. Responses were evoked by linear horizontal and/or vertical accelerations on a sled or by angular accelerations about an earth-vertical axis on a turntable. Before each sinusoidal oscillation test in darkness, the static head position was systematically altered to determine those directions of horizontal linear acceleration and those planes of angular head oscillation that were associated with minimal response amplitudes. Inhibitory response components during angular accelerations were clearly present, whereas inhibitory response components during linear accelerations were absent. Likewise was no contribution from the vertical otolith organs (i.e., lagena and saccule) observed during vertical linear acceleration. Horizontal linear acceleration evoked responses that originated from eye muscle-specific sectors on the contralateral utricular macula. The sectors of the inferior obliquus and lateral rectus muscles on the utricle had an opening angle of 45 and 60 degrees, respectively and overlapped to a large extent in the laterorostral part of the utricle. Both sectors were coplanar with the horizontal semicircular canals. The sector of the inferior rectus muscle was narrow (opening 5 degrees), laterocaudally oriented, and slightly pitched up by 6 degrees. Angular acceleration evoked maximal responses in the inferior obliquus muscle nerve that originated from the ipsilateral horizontal and the contralateral anterior vertical canals in a ratio of 50:50. Lateral rectus excitation originated from the contralateral horizontal and anterior vertical semicircular canals in a ratio of 80:20. The excitatory responses of the inferior rectus muscle nerve originated exclusively from the contralateral posterior vertical canal. Measured data and known semicircular canal plane vectors were used to calculate the spatial orientation of maximum sensitivity vectors for the investigated eye muscle nerves in semicircular canal coordinates. Comparison of the directions of maximal sensitivity vectors of responses evoked by linear or angular accelerations in a given eye muscle nerve showed that the two vector directions were oriented about orthogonally with respect to each other. With this arrangement the linear and the angular vestibuloocular reflex can support each other dynamically whenever they are co-activated without a change in the spatial response characteristics. The mutual adaptation of angular and linear vestibuloocular reflexes as well as the differences in their organization described here for frogs may represent a basic feature common for vertebrates in general.