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Auditory physiology and anatomy of octavolateral efferent neurons in a teleost fish

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Abstract

Vertebrate hair cell systems receive innervation from efferent neurons in the brain. Here we report the responses of octavolateral efferent neurons that innervate the inner ear and lateral lines in a teleost fish, Dormitator latifrons, to directional linear accelerations, and compare them with the afferent responses from the saccule, the main auditory organ in the inner ear of this species. Efferent neurons responded to acoustic stimuli, but had significantly different response properties than saccular afferents. The efferents produced uniform, omnidirectional responses with no phase-locking. Evoked spike rates increased monotonically with stimulus intensity. Efferents were more broadly tuned and responsive to lower frequencies than saccular afferents, and efferent modulation of the otolithic organs and lateral lines is likely more pronounced at lower frequencies. The efferents had wide dynamic ranges, shallow rate-level function slopes, and low maximum discharge rates. These findings support the role of the efferent innervation of the otolithic organs as part of a general arousal system that modulates overall sensitivity of the peripheral octavolateral organs. In addition, efferent feedback may help unmask biologically relevant directional stimuli, such as those emitted by a predator, prey, or conspecific, by reducing sensitivity of the auditory system to omnidirectional ambient noise.

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References

  • Art JJ, Crawford AC, Fettiplace R, Fuchs PA (1982) Efferent regulation of hair cells in the turtle cochlea. Proc R Soc Lond B Biol Sci 216:377–384

    PubMed  CAS  Google Scholar 

  • Art JJ, Fettiplace R, Fuchs PA (1984) Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J Physiol 356:525–550

    PubMed  CAS  Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic, London

    Google Scholar 

  • Boyle R, Highstein SM (1990) Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10:1570–1582

    PubMed  CAS  Google Scholar 

  • Brown MC (1989) Morphology and response properties of single olivocochlear fibers in the guinea pig. Hear Res 40:93–109

    Article  PubMed  CAS  Google Scholar 

  • Buchser WJ, Lu Z, Xu Z, Evoy WH (2003) Frequency response of saccular afferents in a teleost fish. Soc Neurosci Abstr 93.7

  • Chambers JM, Cleveland WS, Kleiner B, Tukey PA (1983) Graphical methods for data analysis. Duxbury Press, Boston

    Google Scholar 

  • Cody AR, Johnstone BM (1982) Temporary threshold shift modified by binaural acoustic stimulation. Hear Res 6:199–205

    Article  PubMed  CAS  Google Scholar 

  • Edds-Walton PL, Fay RR, Highstein SM (1999) Dendritic arbors and central projections of physiologically characterized auditory fibers from the saccule of the toadfish, Opsanus tau. J Comp Neurol 411:212–238

    Article  PubMed  CAS  Google Scholar 

  • Ellaway PH (1978) Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol 45:302–304

    Article  PubMed  CAS  Google Scholar 

  • Fay RR (1984) The goldfish ear codes the axis of acoustic particle motion in three dimensions. Science 225:951–954

    Article  PubMed  CAS  Google Scholar 

  • Fay RR, Edds-Walton PL (1997) Directional response properties of saccular afferents of the toadfish, Opsanus tau. Hear Res 111:1–21

    Article  PubMed  CAS  Google Scholar 

  • Fex J (1962) Auditory activity in centrifugal and centripetal cochlear fibres in cat. A study of a feedback system. Acta Physiol Scand Suppl 189:1–68

    PubMed  CAS  Google Scholar 

  • Fex J (1965) Auditory activity in uncrossed centrifugal cochlear fibres in cat. A study of a feedback system. II. Acta Physiol Scand 64:43–57

    Article  PubMed  CAS  Google Scholar 

  • Flock A, Russell IJ (1973) The post-synaptic action of efferent fibres in the lateral line organ of the burbot Lota lota. J Physiol 35:591–605

    Google Scholar 

  • Flock A, Russell IJ (1976) Inhibition by efferent nerve fibres: action on hair cells and afferent synaptic transmission in the lateral line canal organ of the burbot Lota lota. J Physiol 257:45–62

    PubMed  CAS  Google Scholar 

  • Furukawa T (1981) Effects of efferent stimulation on the saccule of goldfish. J Physiol 315:203–215

    PubMed  CAS  Google Scholar 

  • Galambos R (1956) Suppression of auditory nerve activity by stimulation of efferent fibers to cochlea. J Neurophysiol 19:424–437

    PubMed  CAS  Google Scholar 

  • Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613–636

    PubMed  CAS  Google Scholar 

  • Goldberg JM, Fernandez C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43:986–1025

    PubMed  CAS  Google Scholar 

  • Guinan JJ Jr (1996) Physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds) The Cochlea. Springer, Berlin Heidelberg New York, pp 435–502

    Google Scholar 

  • Hartmann R, Klinke R (1980) Efferent activity in the goldfish vestibular nerve and its influence on afferent activity. Pflugers Arch 388:123–128

    Article  PubMed  CAS  Google Scholar 

  • Highstein SM (1991) The central nervous system efferent control of the organs of balance and equilibrium. Neurosci Res 12:13–30

    Article  PubMed  CAS  Google Scholar 

  • Highstein SM, Baker R (1985) Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. J Neurophysiol 54:370–384

    PubMed  CAS  Google Scholar 

  • Highstein SM, Baker R (1986) Organization of the efferent vestibular nuclei and nerves of the toadfish, Opsanus tau. J Comp Neurol 243:309–325

    Article  PubMed  CAS  Google Scholar 

  • Highstein SM, Kitch R, Carey J, Baker R (1992) Anatomical organization of the brainstem octavolateralis area of the oyster toadfish, Opsanus tau. J Comp Neurol 319:501–518

    Article  PubMed  CAS  Google Scholar 

  • Kawase T, Liberman MC (1993) Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. J Neurophysiol 70:2519–2532

    PubMed  CAS  Google Scholar 

  • Kawase T, Delgutte B, Liberman MC (1993) Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. J Neurophysiol 70:2533–2549

    PubMed  CAS  Google Scholar 

  • Liberman MC (1988) Physiology of cochlear efferent and afferent neurons: direct comparisons in the same animal. Hear Res 34:179–192

    Article  PubMed  CAS  Google Scholar 

  • Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36

    Article  PubMed  CAS  Google Scholar 

  • Locke R, Vautrin J, Highstein S (1999) Miniature EPSPs and sensory encoding in the primary afferents of the vestibular lagena of the toadfish, Opsanus tau. Ann NY Acad Sci 871:35–50

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Popper AN (2001) Neural response directionality correlates of hair cell orientation in a teleost fish. J Comp Physiol A 187:453–465

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Xu Z (2002) Effects of saccular otolith removal on hearing sensitivity of the sleeper goby (Dormitator latifrons). J Comp Physiol A 188:595–602

    Article  CAS  Google Scholar 

  • Lu Z, Xu Z (2004) Response properties of anterior lateral line afferents to acoustic linear acceleration. Soc Neurosci Abstr 530.7

    Google Scholar 

  • Lu Z, Popper AN, Fay RR (1996) Behavioral detection of acoustic particle motion by a teleost fish (Astronotus ocellatus): sensitivity and directionality. J Comp Physiol A 179:227–233

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Song J, Popper AN (1998) Encoding of acoustic directional information by saccular afferents of the sleeper goby, Dormitator latifrons. J Comp Physiol A 182:805–815

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Xu Z, Buchser WJ (2003) Acoustic response properties of lagenar nerve fibers in the sleeper goby, Dormitator latifrons. J Comp Physiol A 189:889–905

    Article  CAS  Google Scholar 

  • Lu Z, Xu Z, Buchser WJ (2004) Coding of acoustic particle motion by utricular fibers in the sleeper goby, Dormitator latifrons. J Comp Physiol A 190:923–938

    CAS  Google Scholar 

  • McCormick CA, Braford MR Jr (1994) Organization of inner ear endorgan projections in the goldfish, Carassius auratus. Brain Behav Evol 43:189–205

    Article  PubMed  CAS  Google Scholar 

  • McCue MP, Guinan JJ Jr (1994a) Acoustically responsive fibers in the vestibular nerve of the cat. J Neurosci 14:6058–6070

    PubMed  CAS  Google Scholar 

  • McCue MP, Guinan JJ Jr (1994b) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J Neurosci 14:6071–6083

    PubMed  CAS  Google Scholar 

  • Meredith GE (1988) Comparative view of the central organization of afferent and efferent circuitry for the inner ear. Acta Biol Hung 39:229–249

    PubMed  CAS  Google Scholar 

  • Meredith GE, Butler AB (1983) Organization of eighth nerve afferent projections from individual endorgans of the inner ear in the teleost, Astronotus ocellatus. J Comp Neurol 220:44–62

    Article  PubMed  CAS  Google Scholar 

  • Nieder PC, Nieder I (1970) Crossed olivocochlear bundle: electrical stimulation enhances masked neural responses to loud clicks. Brain Res 21:135–137

    Article  PubMed  CAS  Google Scholar 

  • Roberts BL, Meredith GE (1989) The efferent system. In: Coombs S, Gorner P, and Munz H (eds) The mechanosensory lateral line. Springer, Berlin Heidelberg New York, pp 445–459

    Google Scholar 

  • Roberts BL, Meredith GE (1992) The efferent innervation of the ear: Variations on an enigma. In: Webster DB, Fay RR, Popper AN (eds) Evolutionary biology of hearing. Springer, Berlin Heidelberg New York, pp 185–210

    Google Scholar 

  • Roberts BL, Russell IJ (1972) The activity of lateral-line efferent neurones in stationary and swimming dogfish. J Exp Biol 57:435–448

    PubMed  CAS  Google Scholar 

  • Robertson D, Gummer M (1985) Physiological and morphological characterization of efferent neurones in the guinea pig cochlea. Hear Res 20:63–67

    Article  PubMed  CAS  Google Scholar 

  • Szucs A (1998) Applications of the spike density function in analysis of neuronal firing patterns. J Neurosci Methods 81:159–167

    Article  PubMed  CAS  Google Scholar 

  • Tomchik SM, Lu Z (2004) Morphology and physiology of otolithic organ efferents. Soc Neurosci Abstr 530.14

  • Tomchik SM, Lu Z (2005) Octavolateral projections and organization in the medulla of a teleost fish, the sleeper goby (Dormitator latifrons). J Comp Neurol 481:96–117

    Article  PubMed  Google Scholar 

  • Tricas TC, Highstein SM (1990) Visually mediated inhibition of lateral line primary afferent activity by the octavolateralis efferent system during predation in the free-swimming toadfish, Opsanus tau. Exp Brain Res 83:233–236

    Article  PubMed  CAS  Google Scholar 

  • Tricas TC, Highstein SM (1991) Action of the octavolateralis efferent system upon the lateral line of free-swimming toadfish, Opsanus tau. J Comp Physiol A 169:25–37

    Article  PubMed  CAS  Google Scholar 

  • Weeg MS, Bass AH (2002) Frequency response properties of lateral line superficial neuromasts in a vocal fish, with evidence for acoustic sensitivity. J Neurophysiol 88:1252–1262

    PubMed  Google Scholar 

  • Weeg MS, Fay RR, Bass AH (2002) Directionality and frequency tuning of primary saccular afferents of a vocal fish, the plainfin midshipman (Porichthys notatus). J Comp Physiol A 188:631–641

    Article  CAS  Google Scholar 

  • Weeg MS, Land BR, Bass AH (2005) Vocal pathways modulate efferent neurons to the inner ear and lateral line. J Neurosci 25:5967–5974

    Article  PubMed  CAS  Google Scholar 

  • Winslow RL, Sachs MB (1987) Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. J Neurophysiol 57:1002–1021

    PubMed  CAS  Google Scholar 

  • Young ED, Robert JM, Shofner WP (1988) Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. J Neurophysiol 60:1–29

    PubMed  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

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Acknowledgements

Support was provided by University of Miami start-up funds, and NIH NIDCD R01DC03275 to ZL and a Robert E. Maytag Fellowship to SMT. We thank Hongsheng Zhang, William Buchser, and Brad Burkett for writing data acquisition and analysis software, Gregory Bigford for assistance with neurophysiology experiments, Ivan Dequesada, Harlee Bustamante, and Sarah Abdelfattah for assistance with histology and cell counts, and Sarah Lim for animal care and maintenance of the aquaria. Lisa Ganser and two anonymous reviewers provided helpful comments on earlier versions of this manuscript. This research is part of a doctoral dissertation to be submitted in partial fulfillment of the requirements for a Ph.D. degree from the University of Miami. Procedures involving animals comply with the Guide for the Care and Use of Laboratory Animals (NIH publication#86–23, revised 1985) and were approved by the University of Miami Animal Care and Use Committee.

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Authors and Affiliations

  1. Department of Biology, University of Miami, 1301 Memorial Drive, Coral Gables, FL, 33146, USA

    Seth M. Tomchik & Zhongmin Lu

  2. Neuroscience Program, University of Miami, Miami, FL, 33101, USA

    Zhongmin Lu

  3. NIEHS Marine and Freshwater Biomedical Sciences Center, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, 33149, USA

    Zhongmin Lu

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  1. Seth M. Tomchik
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Correspondence to Seth M. Tomchik.

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Tomchik, S.M., Lu, Z. Auditory physiology and anatomy of octavolateral efferent neurons in a teleost fish. J Comp Physiol A 192, 51–67 (2006). https://doi.org/10.1007/s00359-005-0050-0

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