Abstract
Sensory adaptation is characterized by a reduction in the firing frequency of neurons to prolonged stimulation, also called spike frequency adaptation. This has been documented for sensory neurons of the visual, olfactory, electrosensory, and auditory system both in response to constant-amplitude and to sinusoidal stimuli, but has thus far not been described systematically for the lateral line system. We recorded neuronal activity from primary afferent nerve fibres in the lateral line in goldfish in response to sinusoidal wave stimuli. Depending on stimulus characteristics, afferent fibre responses exhibited a distinct onset followed by a decline in firing rate to an apparent steady-state level, i.e., they exhibited adaptation. The degree of adaptation, measured as the percent decrease in firing rate between onset and steady-state, increased with stimulus amplitude and frequency and with increasing steepness of the rising flank of the stimulus. This may in part be due to the velocity and/or acceleration sensitivity of the lateral line receptors. The time course of the response decline, i.e., the time course of adaptation was best-fit by a power function. This is consistent with the previous studies on spike frequency adaptation in sensory afferents of weakly electric fish.
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References
Abbott LF, Sen K, Varela JA, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220–222
Adrian ED (1928) The basis of sensation. Christophers, London
Albert J, Nadrowski B, Göpfert MC (2007) Mechanical signatures of transducer gating in Drosophila the ear. Curr Biol 17:1000–1006
Batschelet E (1981) The Rayleigh test. In: Batschelet E (ed) Circular statistics in biology. Academic Press, New York, pp 54–58
Benda J, Herz AVM (2003) A universal model for spike frequency adaptation. Neural Comp 15:2523–2564
Benda J, Tabak J (2014) Spike frequency adaptation. Encyclopedia of Computational Neuroscience, pp 1–12
Benda J, Longtin A, Maler L (2005) Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci 25:2312–2321
Benda J, Maler L, Longtin A (2010) Linear versus nonlinear signal transmission in neuron models with adaptation currents or dynamic thresholds. J Neurophysiol 104:2806–2820
Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. In: Rathmayer W (ed) Progress in zoology, vol 41., Gustav FischerStuttgart, Jena, pp 1–115
Bleckmann H, Weiss O, Bullock TH (1989) Physiology of lateral line mechanoreceptive regions in the elasmobranch brain. J Comp Physiol A 164:459–474
Bleckmann H, Breithaupt T, Blickhan R, Tautz J (1991) The time course and frequency content of hydrodynamic events caused by moving fish, frogs, and crustaceans. J Comp Physiol A 168:749–757
Chagnaud BP, Bleckmann H, Engelmann J (2006) Neural responses of goldfish lateral line afferents to vortex motions. J Exp Biol 209:327–342
Chance FS, Nelson SB, Abbott LF (1998) Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci 18:4785–4799
Clarke SE, Naud R, Lngtin A, Maler L (2013) Speed-invariant encoding of looming object distance requires power law spike rate adaptation. PNAS 110:13624–13629
Coombs S, Conley RA (1997) Dipole source localization by mottled sculpin. I. Approach strategies. J Comp Physiol A 180:387–400
Coombs S, Fay R (1985) Adaptation effects on the detection of amplitude modulation: neurophysiological and behavioral assessment in the goldfish auditory system. Hear Res 19:57–71
Coombs S, Fay R (1987) Response dynamics of goldfish saccular fibers: effects of stimulus frequency and intensity on fibres with different tuning, sensitivity and spontaneous activity. J Acoust Soc Am 81:1025–1035
Coombs S, Janssen J (1990) Behavioral and neurophysiological assessment of lateral line sensitivity in the mottled sculpin, Cottus bairdi. J Comp Physiol A 167:557–567
Coombs S, Montgomery J (1992) Fibres innervating different parts of the lateral line system of the Antarctic fish, Trematomus bernacchii, have similar neural responses despite large variations in peripheral morphology. Brain Behav Evol 40:217–233
Coombs S, Janssen J, Webb J (1988) Diversity of lateral line systems: evolutionary and functional considerations. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 553–594
Coombs S, Hastings M, Finneran J (1996) Modeling and measuring lateral line excitation patterns to changing dipole source locations. J Comp Physiol A 178:359–371
Coombs S, Mogdans J, Halstead M, Montgomery JC (1998) Transformations of peripheral inputs by the first order brainstem nucleus of the lateral line system. J Comp Physiol A 182:609–626
Crumling MA, Saunders JC (2007) Tonotopic distribution of short-term adaptation properties in the cochlear nerve of normal and acoustically overexposed chicks. JARO 8:54–68
Demmer J, Kloppenburg P (2009) Intrinsic membrane properties and inhibitory synaptic input of kenyon cells as mechanisms for sparse coding? J Neurophysiol 102:1538–1550
Elepfandt A, Wiedemer L (1987) Lateral-line responses to water surface waves in the clawed frog, Xenopus laevis. J Comp Physiol A 160:667–682
Engelmann J, Hanke W, Bleckmann H (2002) Lateral line reception in still- and running water. J Comp Physiol A 188:513–526
Engelmann J, Gertz S, Goulet J, Schuh A, von der Emde G (2010) Coding of stimuli by ampullary afferents in Gnathonemus petersii. J Neurophysiol 104:1955–1968
Epping WJM (1990) Influence of adaptation on neural sensitivity to temporal characteristics of sound in the dorsal medullary nucleus and torus semicircularis of the grassfrog. Hear Res 45:1–14
Fay RR (1985) Sound intensity processing by the goldfish. J Acoust Soc Am 78:1296–1309
Finlayson PG, Adam TJ (1997) Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing. Hear Res 103:1–18
Givois V, Pollack GS (2000) Sensory habituation of auditory receptor neurons: implications for sound localization. J Exp Biol 203:2529–2537
Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic stimuli: some physiological implications. J Neurophysiol 32:613–636
Gollisch T, Herz AVM (2004) Input-driven components of spike-frequency adaptation can be unmasked in vivo. J Neurosci 24:7435–7444
Görner P (1963) Untersuchungen zur Morphologie und Elektrophysiologie des Seitenlinienorgans vom Krallenfrosch (Xenopus laevis Daudin). Z vergl Physiol 47:316–338
Harris DM, Dallos P (1979) Forward masking of auditory nerve fibre responses. J Neurophysiol 42:1083–1107
Harris GG, Milne DC (1966) Input–output characteristics of the lateral-line sense organs of Xenopus laevis. JASA 40:32–42
Hudspeth AJ, Choe Y, Mehta AD, Martin P (2000) Putting ion channels to work: mechanoelectrical transduction, adaptation, and amplification by hair cells. Proc Natl Acad Sci 97:11765–11772
Ingham NJ, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91:632–645
Javel E (1996) Long-term adaptation in cat auditory-nerve fibre responses. J Acoust Soc Am 99:1040–1052
Kalmijn AJ (1988) Hydrodynamic and acoustic field detection. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 83–130
Kiang NYS (1965) Discharge patterns of single fibres in the cat’s auditory nerve. MIT Press, Cambridge
Kroese ABA, Schellart NAM (1992) Velocity- and acceleration-sensitive units in the trunk lateral line of the trout. J Neurophysiol 68:2212–2221
Kuno M (1983) Adaptive changes in firing rates in goldfish auditory berve fibres as related to changes in mean amplitude of excitatory postsynaptic potentials. J Neurophysiol 50:573–581
Laughlin SB (1989) The role of sensory adaptation in the retina. J Exp Biol 146:39–62
Megela AL, Capranica RR (1981) Response patterns to tone bursts in peripheral auditory system of anurans. J Neurophysiol 46:465–478
Modrell MS, Bemis WE, Northcutt RG, Davis MC, Baker CVH (2011) Electrosensory ampullary organs are derived from lateral line placodes in bony fishes. Nat Comm 2:496. doi:10.1038/ncomms1502
Mogdans J, Bleckmann H (1999) Peripheral lateral line responses to amplitude-modulated sinusoidal wave stimuli. J Comp Physiol A 185:173–180
Müller U (1984) Anatomische und physiologische Anpassungen des Seitenliniensystems von Pantodon buchholzi an den Lebensraum Wasseroberfläche. PhD thesis, Justus-Liebig-University Gießen
Münz H (1985) Single unit activity in the peripheral lateral line system of the cichlid fish Sarotherodon niloticus L. J Comp Physiol A 157:555–568
Nelson ME, Xu Z, Payne JR (1997) Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish. J Comp Physiol A 181:532–544
Nomoto M, Suga N, Katsuki Y (1964) Discharge pattern and inhibition of primary auditory-nerve fibres in the emonkey. J Neurophysiol 27:768–787
Northcutt G (1989) The phylogenetic distribution and innnervation of craniate mechanoreceptive lateral lines. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, New York, pp 17–78
Oakley B, Schafer R (1978) Experimental neurobiology. The University of Michigan Press, Ann Arbor
Palmer LM, Mensinger AF (2004) Effect of the anesthetic tricaine (MS-222) on nerve activity in the anterior lateral line of the Oyster Toadfish, Opsanus tau. J Neurophysiol 92:1034–1041
Peron S, Gabbiani F (2009) Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci 12:318–326
Rhode WS, Smith PH (1985) Characteristics of tone-pip response patterns in relationship to spontaneous rate in cat auditory nerve fibres. Hear Res 18:159–168
Ronacher B, Hennig RM (2004) Neuronal adaptation improves the recognition of temporal patterns in a grasshopper. J Comp Physiol A 190:311–319
Smith RL (1977) Short-term adaptation in single auditory nerve fibres: some poststimulatory effects. J Neurophysiol 40:1098–1112
Smith RL (1979) Adaptation, saturation, and physiological masking in single auditory nerve fibres. J Acosut Soc Am 65:166–178
Smith RL, Brachman ML (1982) Adaptation in auditory-nerve fibres: a revised model. Biol Cybern 44:107–120
Smith RL, Zwislocki JJ (1975) Short-term adaptation and incremental responses of single auditory-nerve-fibres. Biol Cybern 17:169–182
Späth M, Schweickert W (1977) The effect of metacaine (MS-222) on the activity of the efferent and afferent nerves in the teleost lateral-line system. Naunyn-Schmiedeberg’s Arch Pharmacol 297:9–16
Tasaki I (1954) Nerve impulses in individual auditory nerve fibres of guinea pig. J Neurophysiol 17:97–122
Topp G (1983) Primary lateral line responses to water surface waves in the topminnow Aplocheilus lineatus (Pisces, Cyprinodotinae). Pflügers Arch 397:62–67
Unbehauen H (1980) Morphologische und elektrophysiologische Untersuchungen zur Wirkung von Wasserwellen auf das Seitenorgan des Streifenhechtlings (Aplocheilus lineatus). Dissertation, Eberhard-Karls-Universität Tübingen
van Netten SM (1991) Hydrodynamics of the excitation of the cupula in the fish canal lateral line. JASA 89:310–319
van Netten SM, Kroese AB (1987) Laser interferometric measurements on the dynamic behaviour of the cupula in the fish lateral line. Hear Res 29:55–61
Wark B, Lundstrom BN, Fairhall F (2007) Sensory adaptation. Curr Opin Neurobiol 17:423–429
Webster MA (2012) Evolving concepts of sensory adaptation. F1000 Biol Reports. doi:10.3410/B4-21
Westermann LA, Smith RL (1984) Rapid and short-term adaptation in auditory nerve responses. Hear Res 15:249–260
Wubbels RJ (1992) Afferent response of a head canal neuromast of the ruff (Acerina cernua) lateral line. Comp Biochem Physiol 102:19–26
Wubbels RJ, Kroese ABA, Schellart NAM (1993) Response properties of lateral line and auditory units in the medulla oblongata of the rainbow trout (Oncorhynchus mykiss). J Exp Biol 179:77–92
Xu Z, Payne JR, Nelson ME (1996) Logarithmic time course of sensory adaptation in electrosensory afferent nerve fibers in a weakly electric fish. J Neurophysiol 76:2020–2032
Yates GK, Robertson D, Johnstone BM (1985) Very rapid adaptation in the guinea pig auditory nerve. Hear Res 17:1–12
Zelick R, Narins PM (1985) Temporary threshold shift, adaptation, and recovery characteristics of frog auditory nerve fibres. Hear Res 17:161–176
Acknowledgements
We thank Horst Bleckmann for valuable comments on an earlier version of the manuscript. This research was partly supported by the European Commission, Future and Emerging 476 Technologies, under project CILIA (project number 016039). The experiments reported on in this paper comply with the current animal protection laws of the Federal Republic of Germany (“Tierschutzgesetz”). Use of animals and experimental procedures were approved by the Bezirksregierung Köln, permission no. 50.203.2 BN 7, 14/05.
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Mogdans, J., Müller, C., Frings, M. et al. Adaptive responses of peripheral lateral line nerve fibres to sinusoidal wave stimuli. J Comp Physiol A 203, 329–342 (2017). https://doi.org/10.1007/s00359-017-1172-x
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DOI: https://doi.org/10.1007/s00359-017-1172-x