Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig

• Published in: Experimental brain research Vol. 175; no. 2; pp. 256 - 267
• Main Authors: CURTHOYS, Ian S, KIM, Juno, MCPHEDRAN, Samara K, CAMP, Aaron J
• Format: Journal Article
• Language: English
• Published: Berlin Springer 01.11.2006; Springer Nature B.V
• Subjects: Acoustic Stimulation - methods; Action Potentials - physiology; Animals; Auditory Pathways - physiology; Biological and medical sciences; Biotin - analogs & derivatives; Biotin - metabolism; Bone Conduction - physiology; Ear and associated structures. Auditory pathways and centers. Hearing. Vocal organ. Phonation. Sound production. Echolocation; Evoked Potentials, Auditory, Brain Stem - physiology; Fundamental and applied biological sciences. Psychology; Guinea Pigs; Motor control and motor pathways. Reflexes. Control centers of vegetative functions. Vestibular system and equilibration; Neurons; Neurons, Afferent - classification; Neurons, Afferent - physiology; Otolithic Membrane - physiology; Physiology; Reaction Time - physiology; Semicircular Canals - physiology; Sensory Thresholds - physiology; Vertebrates: nervous system and sense organs; Vestibule, Labyrinth - cytology; Vibration; Saccular; Electrophysiology; Inner ear; Organ of hearing; Guinea pig; Angular acceleration; Vestibular system; Ungulata; Vestibular nerve; Vibration; Rodentia; Discharge pattern; Labyrinth; Stimulus intensity; Sound; Utricular; Pig; Vertebrata; Mammalia; Neuron; Semicircular canal; Otolith; Auditory evoked potential; Skull; Tilt; Artiodactyla; Utricular nerve; Vestibular
• ISSN: 0014-4819; 1432-1106
• DOI: 10.1007/s00221-006-0544-1

The main objective of this study was to determine whether bone-conducted vibration (BCV) is equally effective in activating both semicircular canal and otolith afferents in the guinea pig or whether there is preferential activation of one of these classes of vestibular afferents. To answer this question a large number (346) of single primary vestibular neurons were recorded extracellularly in anesthetized guinea pigs and were identified by their location in the vestibular nerve and classed as regular or irregular on the basis of the variability of their spontaneous discharge. If a neuron responded to angular acceleration it was classed as a semicircular canal neuron, if it responded to maintained roll or pitch tilts it was classified as an otolith neuron. Each neuron was then tested by BCV stimuli-either clicks, continuous pure tones (200-1,500 Hz) or short tone bursts (500 Hz lasting 7 ms)-delivered by a B-71 clinical bone-conduction oscillator cemented to the guinea pig's skull. All stimulus intensities were referred to that animal's own auditory brainstem response (ABR) threshold to BCV clicks, and the maximum intensity used was within the animal's physiological range and was usually around 70 dB above BCV threshold. In addition two sensitive single axis linear accelerometers cemented to the skull gave absolute values of the stimulus acceleration in the rostro-caudal direction. The criterion for a neuron being classed as activated was an audible, stimulus-locked increase in firing rate (a 10% change was easily detectable) in response to the BCV stimulus. At the stimulus levels used in this study, semicircular canal neurons, both regular and irregular, were insensitive to BCV stimuli and very few responded: only nine of 189 semicircular canal neurons tested (4.7%) showed a detectable increase in firing in response to BCV stimuli up to the maximum 2 V peak-to-peak level we delivered to the B-71 oscillator (which produced a peak-to-peak skull acceleration of around 6-8 g and was usually around 60-70 dB above the animal's own ABR threshold for BCV clicks). Regular otolithic afferents likewise had a poor response; only 14 of 99 tested (14.1%) showed any increase in firing rate up to the maximum BCV stimulus level. However, most irregular otolithic afferents (82.8%) showed a clear increase in firing rate in response to BCV stimuli: of the 58 irregular otolith neurons tested, 48 were activated, with some being activated at very low intensities (only about 10 dB above the animal's ABR threshold to BCV clicks). Most of the activated otolith afferents were in the superior division of the vestibular nerve and were probably utricular afferents. That was confirmed by evidence using juxtacellular injection of neurobiotin near BCV activated neurons to trace their site of origin to the utricular macula. We conclude there is a very clear preference for irregular otolith afferents to be activated selectively by BCV stimuli at low stimulus levels and that BCV stimuli activate some utricular irregular afferent neurons. The BCV generates compressional and shear waves, which travel through the skull and constitute head accelerations, which are sufficient to stimulate the most sensitive otolithic receptor cells.