Single neuron activity and c-Fos expression in the rat striatum following electrical stimulation of the peripheral vestibular system

Abstract

Connections between the vestibular system and the basal ganglia have been postulated since the early 20th century. However, the results of electrophysiological studies investigating neuronal responses to electrical stimulation of the vestibular system have been inconsistent. The aim of this study was to investigate the effects of electrical stimulation of the vestibular labyrinth on single neuron activity and c‐Fos expression in the rat striatum. We used electrical stimulation of the vestibular labyrinth (various intensities delivered to the round window) to examine the electrophysiological response of striatal neurons and c‐Fos expression. From 507 single neurons recorded (n = 20 rats), no vestibular‐responsive neuron was found at 1× and 2× the nystagmus threshold; however, 6 neurons were found at 3× the threshold. These neurons were found bilaterally, with a response latency of ~50 msec from the end of the stimulus. For the c‐Fos study, the number of neurons expressing c‐Fos was quantified using stereological methods. Stimulation at 2× the threshold for nystagmus (n = 5 rats) resulted in a significant decrease in the number of neurons expressing c‐Fos in the bilateral striatum compared to both the sham control group (n = 5) and the lower stimulus intensity group (n = 5) (P ≤ 0.0001 for both). The results of this study demonstrate that: (1) some single striatal neurons respond to electrical vestibular stimulation, however, these responses are circumscribed and infrequent; (2) electrical stimulation of the vestibular labyrinth results in a decrease in the number of striatal neurons expressing c‐Fos, in a current‐dependent manner.

The effects of electrical stimulation of the peripheral vestibular system on neurochemical release in the rat striatum

“…A stainless-steel bipolar electrode (MS303/1-B/SPC, Plastics One Inc.), insulated except at the tip, was placed into the round window as the stimulating electrode. It was secured in place using dental cement once the location of the electrode placement was confirmed via visualisation of vestibular nystagmus in response to stimulation, which was considered evidence that the peripheral vestibular system was being adequately activated [ 12 , 39 ] ( Fig 1C ). The surgical site was then sutured closed.…”

“…The surgical site was then sutured closed. Eye movements were recorded using a Dino-Lite microscopic video camera focused on the rat’s eye [ 12 , 39 ], images from which were displayed on a PC monitor. The threshold for nystagmus was defined as the lowest current at which eye movement was visible ( Fig 2 ).…”

“…No stimulation animals received the same surgery but without an electrode implanted. The stimulation was applied for 20 min in each case, based on the results we obtained in our previous study using single neuron recording and c-Fos expression in the striatum [ 12 ]. Microdialysis probe implantation occurred within 1 h of implanting the stimulating electrodes, in order to ensure that the stimulating electrode placement did not change.…”

“…Xylocaine (with 1:10,000 adrenaline; 0.05 ml, s.c) was injected along the midline of the head before an incision was made. Using a dental drill, a small hole was made in the skull to unilaterally expose the area of the brain containing the striatum, either the ipsilateral or contralateral hemisphere to the vestibular stimulating electrode (0.5 mm from bregma and 2–3 mm lateral to the midline) [ 12 , 40 ]; the dura was pierced. A guide cannula (CMA 12 Guide Cannula, CMA microdialysis) was inserted into the brain 6 mm from the top of the skull at a rate of 4 μm/sec.…”

“…Nonetheless, Rancz et al [ 11 ] reported that stimulation of the rat superior vestibular nerve could evoke field potentials and multi-unit activity in the rat striatum, a result that was confirmed using fMRI. In our recent study, we also found that a small population of striatal neurons responded to electrical stimulation of the rat peripheral vestibular system, in a phase-locked manner [ 12 ].These electrophysiological results are consistent with the results from PET and fMRI studies in humans, which have shown increases in activity in the striatum following either caloric or galvanic vestibular stimulation (GVS) [ 13 – 15 ].…”