Journal of Neurophysiology, Vol 51, Issue 6 1236-1256, Copyright © 1984 by APS

ARTICLES

Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey

J. M. Goldberg, C. E. Smith and C. Fernandez

Most vestibular nerve afferents can be classified as regularly or irregularly discharging. Two factors are theoretically identified as being potentially responsible for differences in discharge regularity. The first, ascribable to synaptic noise, is the variance (sigma v2) characterizing the transmembrane voltage fluctuations of the axon's spike trigger site, i.e., the place where impulses normally arise. The second factor is the slope (dmuv/dt) of the trigger site's postspike recovery function. Were (dmuv/dt) a major determinant of discharge regularity, the theory predicts that the more irregular the discharge of a unit, the greater should be its sensitivity to externally applied galvanic currents and the faster should be the postspike recovery of its electrical excitability. The predictions would not hold if differences in the discharge regularity between units largely reflected variations in sigma v. To test these predictions, the responses of vestibular nerve afferents to externally applied galvanic currents were studied in the barbiturate-anesthetized squirrel monkey. Current steps of 5-s duration and short (50 microsecond) shocks were delivered by way of the perilymphatic space of the vestibule. Results were similar regardless of which end organ an afferent innervated. The regularity of discharge of each unit was expressed by a normalized coefficient of variation (CV*). The galvanic sensitivity (beta p) of a unit, measured from its response to current steps, was linearly related to discharge regularity (CV*), there being approximately 20-fold variations in both variables across the afferent population. Various geometric factors--including fiber diameter, position of individual axons within the various nerve branches, and the configuration of unmyelinated processes within the sensory epithelium--are unlikely to have made a major contribution to the positive relation between beta P and CV*. The postspike recovery of electrical excitability was measured as response thresholds to shocks, synchronized to follow naturally occurring impulses at several different delays. Recovery in irregular units was more rapid than in regular units. Evidence is presented that externally applied currents acted at the spike trigger site rather than elsewhere in the sensory transduction process. We argue that the irregular discharge of some vestibular afferents offers no functional advantage in the encoding and transmission of sensory information. Rather, the irregularity of discharge is better viewed as a consequence of the enhanced sensitivity of these units to depolarizing influences, including afferent and efferent synaptic inputs.

This article has been cited by other articles:

				R. A. Eatock, J. Xue, and R. Kalluri Ion channels in mammalian vestibular afferents may set regularity of firing J. Exp. Biol., June 1, 2008; 211(11): 1764 - 1774. [Abstract] [Full Text] [PDF]

				C. Abe, K. Tanaka, C. Awazu, and H. Morita Strong galvanic vestibular stimulation obscures arterial pressure response to gravitational change in conscious rats J Appl Physiol, January 1, 2008; 104(1): 34 - 40. [Abstract] [Full Text] [PDF]

				A. Yang and T. E. Hullar Relationship of Semicircular Canal Size to Vestibular-Nerve Afferent Sensitivity in Mammals J Neurophysiol, December 1, 2007; 98(6): 3197 - 3205. [Abstract] [Full Text] [PDF]

				C. J. Dakin, G. M. L. Son, J. T. Inglis, and J.-S. Blouin Frequency response of human vestibular reflexes characterized by stochastic stimuli J. Physiol., September 15, 2007; 583(3): 1117 - 1127. [Abstract] [Full Text] [PDF]

				J. C. Holt, S. Chatlani, A. Lysakowski, and J. M. Goldberg Quantal and Nonquantal Transmission in Calyx-Bearing Fibers of the Turtle Posterior Crista J Neurophysiol, September 1, 2007; 98(3): 1083 - 1101. [Abstract] [Full Text] [PDF]

				F. Deriu, E. Ortu, S. Capobianco, E. Giaconi, F. Melis, E. Aiello, J. C. Rothwell, and E. Tolu Origin of sound-evoked EMG responses in human masseter muscles J. Physiol., April 1, 2007; 580(1): 195 - 209. [Abstract] [Full Text] [PDF]

				S. G. Sadeghi, L. B. Minor, and K. E. Cullen Response of Vestibular-Nerve Afferents to Active and Passive Rotations Under Normal Conditions and After Unilateral Labyrinthectomy J Neurophysiol, February 1, 2007; 97(2): 1503 - 1514. [Abstract] [Full Text] [PDF]

				S. G. Sadeghi, M. J. Chacron, M. C. Taylor, and K. E. Cullen Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System J. Neurosci., January 24, 2007; 27(4): 771 - 781. [Abstract] [Full Text] [PDF]

				M. S. Welgampola and B. L. Day Craniocentric body-sway responses to 500 Hz bone-conducted tones in man J. Physiol., November 15, 2006; 577(1): 81 - 95. [Abstract] [Full Text] [PDF]

				R. Ramachandran and S. G. Lisberger Transformation of Vestibular Signals Into Motor Commands in the Vestibuloocular Reflex Pathways of Monkeys J Neurophysiol, September 1, 2006; 96(3): 1061 - 1074. [Abstract] [Full Text] [PDF]

				S. T. Aw, M. J. Todd, and G. M. Halmagyi Latency and Initiation of the Human Vestibuloocular Reflex to Pulsed Galvanic Stimulation J Neurophysiol, August 1, 2006; 96(2): 925 - 930. [Abstract] [Full Text] [PDF]

				J.-C. Lepecq, C. De Waele, S. Mertz-Josse, C. Teyssedre, P. T. B. Huy, P.-M. Baudonniere, and P.-P. Vidal Galvanic Vestibular Stimulation Modifies Vection Paths in Healthy Subjects J Neurophysiol, May 1, 2006; 95(5): 3199 - 3207. [Abstract] [Full Text] [PDF]

				M. Cenciarini and R. J. Peterka Stimulus-Dependent Changes in the Vestibular Contribution to Human Postural Control J Neurophysiol, May 1, 2006; 95(5): 2733 - 2750. [Abstract] [Full Text] [PDF]

				S. M. Highstein, R. D. Rabbitt, G. R. Holstein, and R. D. Boyle Determinants of Spatial and Temporal Coding by Semicircular Canal Afferents J Neurophysiol, May 1, 2005; 93(5): 2359 - 2370. [Abstract] [Full Text] [PDF]

				F. Deriu, E. Tolu, and J. C. Rothwell A Sound-Evoked Vestibulomasseteric Reflex in Healthy Humans J Neurophysiol, May 1, 2005; 93(5): 2739 - 2751. [Abstract] [Full Text] [PDF]

				T. E. Hullar, C. C. Della Santina, T. Hirvonen, D. M. Lasker, J. P. Carey, and L. B. Minor Responses of Irregularly Discharging Chinchilla Semicircular Canal Vestibular-Nerve Afferents During High-Frequency Head Rotations J Neurophysiol, May 1, 2005; 93(5): 2777 - 2786. [Abstract] [Full Text] [PDF]

				K. P. Maruska and T. C. Tricas Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray J. Exp. Biol., September 15, 2004; 207(20): 3463 - 3476. [Abstract] [Full Text] [PDF]

				L. R. Bent, J. T. Inglis, and B. J. McFadyen When is Vestibular Information Important During Walking? J Neurophysiol, September 1, 2004; 92(3): 1269 - 1275. [Abstract] [Full Text] [PDF]

				R. C. Fitzpatrick and B. L. Day Probing the human vestibular system with galvanic stimulation J Appl Physiol, June 1, 2004; 96(6): 2301 - 2316. [Abstract] [Full Text] [PDF]

				M. A. Vollrath and R. A. Eatock Time Course and Extent of Mechanotransducer Adaptation in Mouse Utricular Hair Cells: Comparison With Frog Saccular Hair Cells J Neurophysiol, October 1, 2003; 90(4): 2676 - 2689. [Abstract] [Full Text] [PDF]

				C. A. Livingston and S. R. Fedder Visual-Ocular Motor Activity in the Macaque Pregeniculate Complex J Neurophysiol, July 1, 2003; 90(1): 226 - 244. [Abstract] [Full Text] [PDF]

				J. D. Hunter and J. G. Milton Amplitude and Frequency Dependence of Spike Timing: Implications for Dynamic Regulation J Neurophysiol, July 1, 2003; 90(1): 387 - 394. [Abstract] [Full Text] [PDF]

				K. Jahn, A. Naessl, E. Schneider, M. Strupp, T. Brandt, and M. Dieterich Inverse U-shaped curve for age dependency of torsional eye movement responses to galvanic vestibular stimulation Brain, July 1, 2003; 126(7): 1579 - 1589. [Abstract] [Full Text] [PDF]

				A. M. Brichta, A. Aubert, R. A. Eatock, and J. M. Goldberg Regional Analysis of Whole Cell Currents From Hair Cells of the Turtle Posterior Crista J Neurophysiol, December 1, 2002; 88(6): 3259 - 3278. [Abstract] [Full Text] [PDF]

				J. D. Dickman and D. E. Angelaki Vestibular Convergence Patterns in Vestibular Nuclei Neurons of Alert Primates J Neurophysiol, December 1, 2002; 88(6): 3518 - 3533. [Abstract] [Full Text] [PDF]

				M. Plotnik, V. Marlinski, and J. M. Goldberg Reflections of Efferent Activity in Rotational Responses of Chinchilla Vestibular Afferents J Neurophysiol, September 1, 2002; 88(3): 1234 - 1244. [Abstract] [Full Text] [PDF]

				B. L. Day and J. Cole Vestibular-evoked postural responses in the absence of somatosensory information Brain, September 1, 2002; 125(9): 2081 - 2088. [Abstract] [Full Text] [PDF]

				K. E. Cullen and L. B. Minor Semicircular Canal Afferents Similarly Encode Active and Passive Head-On-Body Rotations: Implications for the Role of Vestibular Efference J. Neurosci., May 30, 2002; (2002) 20026418. [Abstract] [Full Text] [PDF]

				E. Schneider, S. Glasauer, and M. Dieterich Comparison of Human Ocular Torsion Patterns During Natural and Galvanic Vestibular Stimulation J Neurophysiol, April 1, 2002; 87(4): 2064 - 2073. [Abstract] [Full Text] [PDF]

				H. G. MacDOUGALL, A. E. BRIZUELA, I. S. CURTHOYS, and G. M. HALMAGYI Three-Dimensional Eye-Movement Responses to Surface Galvanic Vestibular Stimulation in Normal Subjects and in Patients: A Comparison Ann. N.Y. Acad. Sci., April 1, 2002; 956(1): 546 - 550. [Full Text] [PDF]

				R. McCREA, G. GDOWSKI, and H. LUAN Current Concepts of Vestibular Nucleus Function: Transformation of Vestibular Signals in the Vestibular Nuclei Ann. N.Y. Acad. Sci., October 1, 2001; 942(1): 328 - 344. [Abstract] [Full Text] [PDF]

				F. B. Horak and F. Hlavacka Somatosensory Loss Increases Vestibulospinal Sensitivity J Neurophysiol, August 1, 2001; 86(2): 575 - 585. [Abstract] [Full Text] [PDF]

				L. Ris, M. Hachemaoui, N. Vibert, E. Godaux, P. P. Vidal, and L. E. Moore Resonance of Spike Discharge Modulation in Neurons of the Guinea Pig Medial Vestibular Nucleus J Neurophysiol, August 1, 2001; 86(2): 703 - 716. [Abstract] [Full Text] [PDF]

				C. Chabbert, J. M. Chambard, A. Sans, and G. Desmadryl Three Types of Depolarization-Activated Potassium Currents in Acutely Isolated Mouse Vestibular Neurons J Neurophysiol, March 1, 2001; 85(3): 1017 - 1026. [Abstract] [Full Text] [PDF]

				S. Bense, T. Stephan, T. A. Yousry, T. Brandt, and M. Dieterich Multisensory Cortical Signal Increases and Decreases During Vestibular Galvanic Stimulation (fMRI) J Neurophysiol, February 1, 2001; 85(2): 886 - 899. [Abstract] [Full Text] [PDF]

				D. E. Angelaki and J. D. Dickman Spatiotemporal Processing of Linear Acceleration: Primary Afferent and Central Vestibular Neuron Responses J Neurophysiol, October 1, 2000; 84(4): 2113 - 2132. [Abstract] [Full Text] [PDF]

				A. M. Brichta and J. M. Goldberg Morphological Identification of Physiologically Characterized Afferents Innervating the Turtle Posterior Crista J Neurophysiol, March 1, 2000; 83(3): 1202 - 1223. [Abstract] [Full Text] [PDF]

				A. M. Brichta and J. M. Goldberg Responses to Efferent Activation and Excitatory Response-Intensity Relations of Turtle Posterior-Crista Afferents J Neurophysiol, March 1, 2000; 83(3): 1224 - 1242. [Abstract] [Full Text] [PDF]

				D. E. Angelaki, M. Q. McHenry, J. D. Dickman, and A. A. Perachio Primate Translational Vestibuloocular Reflexes. III. Effects of Bilateral Labyrinthine Electrical Stimulation J Neurophysiol, March 1, 2000; 83(3): 1662 - 1676. [Abstract] [Full Text] [PDF]

				D. E. ANGELAKI, M. Q. McHENRY, S. D. NEWLANDS, and J. D. DICKMAN Functional Organization of Primate Translational Vestibulo-Ocular Reflexes and Effects of Unilateral Labyrinthectomy Ann. N.Y. Acad. Sci., May 28, 1999; 871(1): 136 - 147. [Abstract] [Full Text] [PDF]

				E. LOBEL, J. F. KLEINE, A. LEROY-WILLIG, P.-F. VAN DE MOORTELE, D. LE BIHAN, O.-J. GRUSSER, and A. BERTHOZ Cortical Areas Activated by Bilateral Galvanic Vestibular Stimulation Ann. N.Y. Acad. Sci., May 28, 1999; 871(1): 313 - 323. [Abstract] [Full Text] [PDF]

				E. Lobel, J. F. Kleine, D. L. Bihan, A. Leroy-Willig, and A. Berthoz Functional MRI of Galvanic Vestibular Stimulation J Neurophysiol, November 1, 1998; 80(5): 2699 - 2709. [Abstract] [Full Text] [PDF]

				J. D. Hunter, J. G. Milton, P. J. Thomas, and J. D. Cowan Resonance Effect for Neural Spike Time Reliability J Neurophysiol, September 1, 1998; 80(3): 1427 - 1438. [Abstract] [Full Text] [PDF]

				A. M. Brichta and J. M. Goldberg The Papilla Neglecta of Turtles: A Detector of Head Rotations with Unique Sensory Coding Properties J. Neurosci., June 1, 1998; 18(11): 4314 - 4324. [Abstract] [Full Text] [PDF]

				S. F. Myers, H. H. Salem, and J. A. Kaltenbach Efferent Neurons and Vestibular Cross Talk in the Frog J Neurophysiol, April 1, 1997; 77(4): 2061 - 2070. [Abstract] [Full Text] [PDF]