Selective Activation of Vestibular Hair Cells by Infrared Light

Abstract

Optical stimulation using pulsed infrared light is novel method with potential for selectively stimulating a small group of neurons. In present study, we show that infrared light can selectively activate vestibular hair cells and may offer a novel method to investigate biophysical mechanisms underlying the response. In experiments conducted in toadfish, O. tau, horizontal semicircular canal afferents showed a mix of inhibitory and excitatory responses evoked by infrared radiation. In a subset of afferents the background discharge rate decreased, while in other afferents the background discharge rate increased with infrared radiation. Excitatory vs. inhibitory afferent responses correlated with the dynamic adaptive properties of afferent responses observed during mechanical stimuli. Primary semicircular canal afferents in the toadfish are known to receive convergent inhibitory (GABA) and excitatory (glutamate) synaptic input from hair cells that ultimately shape the afferent discharge response. The present data indicate that afferents known to synapse on glutamatergic hair cells increase their discharge rate with incident infrared light, consistent with depolarization of hair cells and increased tonic release of glutamate. Acceleration-coding afferents which synapse on combinations of Glutamatergic and GABAergic hair cells were observed to reduce their discharge rate with infrared light, again indicating depolarization of hair cells but, in this case the inhibition was consistent with increased release of GABA. Repeated optical radiation elicited depolarization/repolarization of hair cells. Sensitive afferents were observed to phase-lock their discharge with the pulsed light stimulation. Since the entire epithelium was irradiated, this argues against simple kT thermodynamic modulation of hair cell channel kinetics. The results compel the hypotheses that infrared light stimulation increases the open probability of IR-sensitive ion channels and depolarizes hair cells due to the influx of cations. [Supported by NIH R01 DC06685 (Rabbitt, RD) and NIH grant 1R41DC008515-02 (Richter, CP)].