Summary
Extracellular recording from single auditory nerve fibers in the pigeon,Columba livia, revealed some unusual discharge patterns of spontaneous and evoked activity.
Time interval histograms (TIHs) of spontaneous activity showed a random interval distribution in 73% of the auditory fibers (Fig. 1a). The remaining 27% revealed periodicity in the TIHs (Fig. 1b–e), determined by the characteristic frequency (CF) of a given fiber. Normally, those fibers had a CF<2.2 kHz. In both cases spontaneous activity was irregular.
The time pattern of quasiperiodic spontaneous firing in different auditory fibers is described by three main types of autocorrelation histograms (ACHs; decaying, nondecaying, and modulated), reflecting the spontaneous oscillations of the hair cell membrane potential (Fig. 1b–d).
Single-tone suppression in auditory fibers with quasi-periodic spontaneous activity was found (Figs. 2, 10) and it could be observed if the eighth nerve was cut. There was no suppressive effect in fibres with random spontaneous firing.
The frequency selectivity properties of auditory fibers were studied by means of an automatic method. Both ‘simple’ (Fig. 4) and ‘complex’ (Figs. 7, 8) response maps were found. Apart from the usual excitatory area, complex response maps were characterized by suppressive areas lying either above (Fig. 7), below (Fig. 8e), or on both sides of the CF (Fig. 8a–c). Generally, complex response maps were observed for fibers showing quasiperiodic spontaneous activity (Figs. 7, 8).
Input-output functions at frequencies evoking single-tone suppression were nonmonotonic, while they were always monotonic at frequencies near the CF (Fig. 12).
No difference in sharpness was observed between normal frequency threshold curves (FTCs) and exitatory areas of ‘complex’ response maps (Fig. 9).
‘On-off’ responses evoked by suppressive stimuli were found (Figs. 2, 3). They had a periodic pattern determined by the CF and did not depend on the stimulus frequency (Fig. 3).
Low-CF fibers were observed which changed their time discharge structure to tone levels about 45 dB lower than their thresholds at the CF (Fig. 6).
The observed features of the discharge patterns of the pigeon's auditory fibers reflect the distinctive nature of the fundamental mechanisms of auditory analysis in birds that are connected with electrical tuning of the hair cells and probably with the micromechanics of the bird's cochlea.
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Abbreviations
- ACH :
-
autocorrelation histogram
- BP :
-
base period
- CF :
-
characteristic frequency
- FTC :
-
frequency threshold curve
- IHC :
-
inner hair cell
- OHC :
-
outer hair cell
- PSTH :
-
peristimulus time histogram
- TIH :
-
time interval histogram
References
Art JJ, Crawford AC, Fettiplace RR (1986) Electrical resonance and membrane currents in the turtle cochlear hair cells. Hearing Res 22:31–36
Arthur RM, Pfeiffer RR, Suga N (1971) Properties of ‘two-tone inhibition’ in primary auditory neurones. J Physiol (Lond) 212:593–609
Ashmore JF (1983) Frequency tuning in a frog vestibular organ. Nature 304:536–538
Ashmore JF, Bronwell WE (1986) Kilohertz movements inducted by electrical stimulation in outer hair cells isolated from guinea-pig cochlea. J Physiol (Lond) 377:41P
Békésy G von (1944) Über die mechanische Frequenzanalyse in der Schnecke verschiedener Tiere. Akust Z 9:3–11
Boord RL (1964) The number and diameter of myelinated fibers in stato-acoustic nerve of the adult pigeon. Am Zool 4:101
Boord RL, Rasmussen GL (1963) Projection of cochlear and lagenar nerves on the cochlear nuclei of the pigeon. J Comp Neurol 120:463–473
Capranica RR (1976) Morphology and physiology of the auditory system. In: Linás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 551–575
Crawford AC, Fettiplace RR (1980) The frequency selectivity of auditory nerve fibers and hair cells in the cochlea of the turtle. J Physiol (Lond) 306:79–125
Crawford AC, Fettiplace RR (1981) An electrical tuning mechanism in cochlear cells in turtle. J Physiol (Lond) 312:377–412
Crawford AC, Fettiplace RR (1985) The mechanical properties of ciliary bundles of the turtle cochlear hair cells. J Physiol (Lond) 364:359–379
Dallos P (1985) Response characteristics of mammalian cochlear hair cells. J Neurosci 5:1591–1608
Dallos P, Harris D (1978) Properties of auditory nerve responses in absence of outer hair cells. J Neurophysiol 41:365–385
Dohlman CF (1971) The attachment of cupulae, otolith and tectorial membrane to the sensory cell areas. Acta Otolaryngol 71:89–105
Eatock RA, Manley GA, Pawson L (1981) Auditory nerve fiber activity in the Tokay Gecko: I. Implications for cochlear processing. J Comp Physiol 142:203–218
Evans EF (1972) The frequency response and other properties in the guinea-pig auditory nerve. J Physiol (Lond) 226:263–287
Evans EF (1979) Single unit studies of mammalian cochlear nerve. In: Beagley HA (ed) Auditory investigation: the scientific and technological basis. Oxford, pp 324–367
Evans EF, Klinke R (1982) The effects of intracochlear and systemic furosemide on the properties of single cochlear nerve fibers in the cat. J Physiol (Lond) 331:409–427
Feng AS, Narins PM, Capranica RR (1975) Three populations of primary auditory fibers in bullfrog (Rana catesbeiana): their peripheral origin and frequency selectivity. J Comp Physiol 100:221–229
Flock A (1965) Transducting mechanisms in the lateral line canal organ receptors. Cold Spring Harb Symp Quant Biol 30:133–145
Flock A (1971) Sensory transduction in hair cells. In: Loewenstein (ed) Principles of receptor physiology (Handbook of sensory physiology, vol 1) Springer, Berlin Heidelberg New York, pp 396–401
Flock A, Cheung H (1977) Actin filaments in sensory hairs of the inner ear receptor cells. J Cell Biol 75:339–343
Flock A, Flock B, Ulfendahl M (1986) Mechanisms of movement in outer hair cells and a possible structural basis. Arch Otorhinolaryngol 243:83–90
Frederiksen E (1977) Condenser microphones used as sound sources. Techn Rev Brüel & Kjaer 3:3–28
Golubeva TB (1985a) Development of bird's hearing in ontogeny (in Russian). Doctoral Dissertation, Moscow State University
Golubeva TB (1985b) The structural organization of the receptor part in the bird's cochlea. In: Barsova LI, Vassiljev BD, Bogoslovskaja LS (eds) Auditory centers of medulla oblongata in terrestrial vertebrates (in Russian). Nauka Moscow, pp 42–51
Golubeva TB, Tichonov AV (1985) The voice and hearing of birds in ontogeny. Acta XVIII Ornithol Congr Moscow, pp 259–274
Golubeva TB, Yamalova GV (1980) Structure-functional features of peripheral part of bird's auditory system. In: Ilyichev VD, Bogoslovskaja LS (eds) Sensory systems and brain of birds (in Russian). Nauka, Moscow, pp 84–113
Goodley LB, Boord RL (1966) Quantitative analysis of the hair cells of the auditory papilla of the pigeon. Am Zool 6:542
Gross NB, Anderson DJ (1976) Single unit responses recorded from first order neuron of pigeon auditory system. Brain Res 101:209–222
Heiligenberg W, Bastian J (1984) The electric sense of weakly electric fish. Annu Rev Physiol 46:561–583
Hillery CM, Narins PM (1984) Neurophysiological evidence for a traveling wave in the amphibian inner ear. Science 225:1037–1039
Hind JE, Anderson DJ, Brugge JF, Rose JE (1967) Time structure of discharges in single auditory fibers of squirrel monkey in response to complex periodic sound. J Neurophysiol 32:368–401
Holton T (1980) Relation between frequency selectivity and two-tone rate suppression in lizard cochlear nerve fibers. Hearing Res 2:21–38
Holton T, Weiss TF (1978) Two-tone rate suppression in lizard nerve fibers, relation to receptor morphology. Brain Res 159:219–222
Hudspeth AJ (1983) Transduction and tuning by vertebrate hair cells. Trends on Neurosci 6:366–369
Hudspeth AJ (1986) The ionic channels of a vertebrate hair cell. Hearing Res 22:21–28
Kiang NY-S (1965) Discharge patterns of single fibers in the cat's auditory nerve. MIT Press, Cambridge, Mass
Klinke R (1985) Function of inner ear — present concept. Pflügers Arch 403 [Suppl 221]:R4
Klinke R, Pause M (1980) Discharge properties of primary auditory fibers inCaiman crocodilus: comparisons and contrasts to the mammalian auditory nerve. Exp Brain Res 38:137–150
Klinke R, Schermuly L (1986) Inner ear mechanics of crocodilian and avian basilar papillae in comparison to neuronal data. Hearing Res 22:183–184
Klinke R, Smolders JWT (1984) Hearing mechanisms in caiman and pigeon. In: Boils L, Keynes RD, Maddrell SHP (eds) Comparative physiology of sensory systems. Cambridge University Press, Cambridge pp 195–211
Lewis RS, Hudspeth AJ (1983) Voltage- and ion-dependent conductance in solitary vertebrate hair cells. Nature 304:538–541
Liff H (1970) Phase dependence of two-tone inhibition in frog auditory nerve fibers. J Acust Soc Am 47:68
Manley GA (1979) Preferred intervals in spontaneous activity of primary auditory neurons. Naturwissenschaften 66:582–583
Manley GA (1981) A review of the auditory physiology of reptiles. Progr Sensory Physiol 2:49–134
Manley GA (1983) Auditory nerve fiber activity in mammals. In: Lewis B (ed) Bioacustics. Springer, Berlin Heidelberg New York Tokyo, pp 207–232
Manley GA, Gleich O (1984) Avian primary auditory neurones: the relationship between characteristic frequency and preferred intervals. Naturwissenschaften 71:592–594
Manley GA, Leppelsack H-J (1977) Preliminary data on activity patterns of cochlear ganglion neurones in starling. INSERM, Paris, pp 127–136
Manley GA, Gleich O, Leppelsack H-J, Oeckinghaus H (1985) Activity patterns of cochlear ganglion neurones in the starling. J Comp Physiol A 157:161–181
Møller AR (1970) The use of correlation analysis in processing neuroelectric data. Progr Brain Res 33:87–100
Molnar CE, Loeffel RG, Pfeiffer RR (1968) Distortion compensating, condenser-earphone driver for physiological studies. J Acoust Soc Am 43:1177–1178
Mulroy MJ, Altmann DW, Weiss TF, Peake WT (1974) Intracellular electric responses to sound in a vertebrate cochlea. Nature 249:482–485
Necker R (1970) Zur Entstehung der Cochleapotentiale von Vögeln: Verhalten bei O2-Mangel, Cyanidvergiftung und Unterkühlung sowie Beobachtungen über die räumliche Verteilung. Z Vergl Physiol 69:367–425
Oeckinghaus H (1985) Modulation of activity in starling cochlear ganglion units by middle-ear muscle contractions, perilymph movements and lagena stimuli. J Comp Physiol A 157:643–655
Oldfield BP (1985) The tuning of auditory receptors in bushcrickets. Hearing Res 17:27–35
Powell FL (1983) Respiration. In: Abs M (ed) Physiology and behavior of the pigeon. Academic Press, London, pp 73–95
Rhode WS, Geisler CD, Kennedy DK (1978) Auditory nerve responses to wide-band noise and tone combinations. J Neurophysiol 41:692–704
Russel IJ, Sellick PM (1978) Intacellular studies of hair cells in the mammalian cochlea. J Physiol (Lond) 284:261–290
Ryals BM, Rubel WR (1982) Patterns of hair cell loss in chick basilar papilla after intense auditory stimulation. Acta Otolaryngol 93:31–41
Ryals BM, Rubel WR (1985) Ontogenetic changes in the position of hair cell loss after acoustic overstimulation in avian basilar papilla. Hearing Res 19:135–142
Sachs MB, Kiang NY-S (1968) Two-tone inhibition in auditory neuron nerve fibers. J Acoust Soc Am 45:1025–1036
Sachs MB, Young ED, Lewis RH (1974) Discharge patterns of single fibers in the pigeon auditory nerve. Brain Res 70:431–447
Sachs MB, Woolf NK, Sinnott JM (1980) Response properties of neurons in the avian auditory system: comparisons with mammalian homologues and consideration of the neural encoding of complex stimuli. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, pp 323–353
Schermuly L, Klinke R (1982) Tuning properties of pigeon primary auditory afferents depend on temperature. Pflügers Arch 394 [Suppl 63]:226
Schermuly L, Klinke R (1985) Change of characteristic frequency of pigeon primary auditory afferents with temperature. J Comp Physiol A 156:209–211
Schermuly L, Göttle K-H, Klinke R (1983) Little ototoxic effect of furosemide on the pigeon inner ear. Hearing Res 10:279–282
Schwartzkopff J (1973) Mechanoreception. In: Farner DC, King J (eds) Avian biology, vol 3. Academic, New York pp 417–477
Sellick PM, Russel IJ (1979) Two-tone suppression in cochlear hair cells. Hearing Res 1:227–236
Sellick PM, Pattuzzi R, Johnstone BM (1982) Measurement of basilar membrane motion in the guinea pig using the Mössbauer technique. J Acoust Soc Am 72:131–141
Smith CA (1981) Recent advances in structural correlates of auditory receptors. Progr Sensory Physiol 2:135–187
Smolders JWT, Klinke R (1984) Effects of temperature on properties of primary auditory fibers of the spectacled caiman,Caiman crocodilus (L.). J Comp Physiol A 155:19–30
Smolders JWT, Gummer AW, Klinke R (1986) Travelling wave motion along the pigeon basilar membrane. Otorhinolaryngol 48:93–97
Strelioff D, Flock A, Minser KE (1985) Role of inner and outer cells in mechanical frequency selectivity of the cochlea. Hearing Res 18:169–175
Takasaka T, Smith CA (1971) The structure and innervation of the pigeon's basilar papillae. J Ultrastruct Res 35:20–65
Tanaka K, Smith CA (1975) Structure of the avian tectorial membrane. Ann Otol Rhinol Laryngol 84:287–297
Tanaka K, Smith CA (1978) Structure of chicken's inner ear: SEM and TEM study. Am J Anat 153:251–272
Temchin AN (1972) Phase-sensitivity of peripheral levels of auditory system in birds (in Russian). Fiziol Zh SSSR 58:1558–1568
Temchin AN (1980a) Functional properties of auditory nerve fibers in pigeon. In: Ilyichev VD, Bogoslovskaja LS (eds) Sensory systems and brain of birds (in Russian). Nauka, Moscow, pp 139–165
Temchin AN (1980b) Multimodality of the interspike distribution of spontaneous activity in pigeon's auditory nerve fibers (in Russian). Dokl Akad Nauk SSSR 253:743–747
Temchin AN (1980c) Afferent inhibition in single auditory nerve fibers in pigeon (in Russian). Dokl Akad Nauk SSSR 253:1272–1275
Temchin AN (1982) Some functional features of auditory nerve fibers in birds. In: Gershuni GV (ed) Sensory systems (in Russian). Nauka, Leningrad, pp 159–169
Temchin AN (1983) Spontaneous activity in pigeon's auditory nerve fibers (in Russian) Fiziol Zh SSSR 59:26–33
Temchin AN (1985a) Acoustical reception in birds. Acta XVIII Ornithol Congr Moscow, pp 275–281
Temchin AN (1985b) Frequency properties of one-tone inhibition of single auditory nerve fibers in pigeon (in Russian). Dokl Akad Nauk SSSR 285:252–256
Tilney LG, Saunders JC (1983) Actin filaments, stereocilia and hair cells of the bird cochlea. J Cell Biol 96:807–834
Viancour TA (1979) Electroreceptors of weakly electric fish. J Comp Physiol 133:317–338
Walsh BT, Miller JB, Gacek RR, Kiang NY-S (1972) Spontaneous activity in the eighth cranial nerve of the cat. Int J Neurosci 3:221–236
Weiss TF (1982) Bidirectional transduction in vertebrate hair cells: a mechanism for coupling mechanical and electrical processes. Hearing Res 7:353–360
Weiss TF, Leong R (1985) A model for signal transmission in an ear having hair cells with free-standing stereocilia. IV. Mechanoelectric transduction stage. Hearing Res 20:175–195
Wilson JP, Smolders JWT, Klinke R (1985) Mechanics of the basilar membrane inCaiman crocodilus. Hearing Res 18:1–14
Zwislocki JJ (1975) Phase opposition between inner and outer hair cells and auditory sound analysis. Audiology 14:443–455
Zwislocki JJ (1986) Analysis of cochlear mechanics. Hearing Res 22:155–169
Zwislocki JJ, Kletsky EJ (1979) Tectorial membrane: a possible effect on frequency analysis in the cochlea. Science 204:639–641
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Temchin, A.N. Unusual discharge patterns of single fibers in the pigeon's auditory nerve. J. Comp. Physiol. 163, 99–115 (1988). https://doi.org/10.1007/BF00612001
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DOI: https://doi.org/10.1007/BF00612001