Responses to Somatosensory Input by Afferent and Efferent Neurons in the Vestibular Nerve of the Frog

Abstract

In the frog, we have recorded the activity of efferent and afferent fibers in the nerve of the horizontal semicircular canal in response to somatosensory stimulation. Recordings were made extracellularly by means of glass micropipettes filled with 2 M NaCl, and somatosensory stimulation was produced either by electrical stimulation of the sciatic nerve (ipsi- or contralateral to the recording side) or by vibratory stimulation of the gastrocnemius. The discharge frequency of 43 % of the efferent fibers recorded was significantly increased by such stimulation, while the activity of the others was unaffected. The discharge rate of the afferent fibers was either significantly increased (in about 11 % of the cases when the results were pooled together) or significantly decreased (in about 22% of the cases) by stimulation of the somatosensory system. The latencies of the responses ranged from 5 to 50 ms. These results show that: (1) somatosensory input can influence the activity of the vestibular apparatus at the most peripheral level; (2) modulation of the afferent discharge is mediated by the efferent vestibular system (EVS); (3) the influence of the EVS on the vestibular afferent activity is both inhibitory and facilitatory, and (4) the responses to somatosensory stimulation are mediated by both long-latency polysynaptic and short-latency oligosynaptic pathways. The functional significance of these two pathways is discussed.

Reviewing the Role of the Efferent Vestibular System in Motor and Vestibular Circuits

“…Although, this study implicates the EVN in mediating changes to contralateral vestibular nuclei interactions that occur at the level of peripheral sensors, the classification of recorded neurons was not conclusive (for example, retrograde staining of recorded neurons was not performed to confirm their locations), and therefore provides a caveat to their results. However, in addition to canal stimulation, a significant increase in the discharge rate of 40% of peripheral efferent fibers was observed in response to sciatic nerve stimulation in the frog (Caston and Bricout-Berthout, 1984 ), suggesting that the function of the EVN may be linked to the spinal circuits underlying locomotion, a potential functional role elaborated further in Section The EVS Signals Corollary Discharge between Vestibular and Other CNS Structures.…”

Differences in the Structure and Function of the Vestibular Efferent System Among Vertebrates

“…Classic studies in fish ( Figure 2A ) demonstrated that somatosensory stimulation activates individual vestibular afferents ( Hartmann and Klinke, 1980 ; Highstein and Baker, 1985 ), and that visual stimulation can evoke directionally sensitive responses ( Klinke, 1970 ). Likewise, somatosensory and visual stimulation has also been reported to alter the firing activity of individual vestibular afferents in amphibians ( Figure 2B ; frog: Caston and Bricout-Berthout, 1982 , 1984 , respectively). Yet, in this latter vertebrate class, somatosensory stimulation can both inhibit and excite afferents, and thus contrasts with what is seen in fish.…”

Neural substrates underlying vestibular compensation: Contribution of peripheral versus central processing

“…The findings of prior investigations in frog had suggested that extravestibular signals (e.g., somatosensory, proprioceptive, and/or motor efference copy signals) transmitted through efferent neurons can be used to change afferent responses under specific behavioral conditions (Bricout-Berthout et al 1984; Caston and Bricout-Berthout 1984; Precht et al 1971; Schmidt 1963). Thus, we also tested this possibility by characterizing afferent responses to such extravestibular signals during passive stimulation of neck somatosensory and proprioceptive inputs, as well as during active head movements during which a command to move the head was produced (Sadeghi et al 2007).…”