Summary
The functional role of GABA and glycine in monaural and binaural signal analysis was studied in single unit recordings from the central nucleus of the inferior colliculus (IC) of horseshoe bats (Rhinolophus rouxi) employing microiontophoresis of the putative neurotransmitters and their antagonists bicuculline and strychnine.
Most neurons were inhibited by GABA (98%; N=107) and glycine (92%; N=118). Both neurotransmitters appear involved in several functional contexts, but to different degrees.
Bicuculline-induced increases of discharge activity (99% of cells; N=191) were accompanied by changes of temporal response patterns in 35% of neurons distributed throughout the IC. Strychnine enhanced activity in only 53% of neurons (N=147); cells exhibiting response pattern changes were rare (9%) and confined to greater recording depths. In individual cells, the effects of both antagonists could markedly differ, suggesting a differential supply by GABAergic and glycinergic networks.
Bicuculline changed the shape of the excitatory tuning curve by antagonizing lateral inhibition at neighboring frequencies and/or inhibition at high stimulation levels. Such effects were rarely observed with strychnine.
Binaural response properties of single units were influenced either by antagonization of inhibition mediated by ipsilateral stimulation (bicuculline) or by changing the strength of the main excitatory input (bicuculline and strychnine).
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Abbreviations
- BF :
-
best frequency
- Bic :
-
bicuculline
- C :
-
control
- CF :
-
constant frequency
- CN :
-
cochlear nucleus
- DNLL :
-
dorsal nucleus of the lateral lemniscus
- FM :
-
frequency modulation
- GABA :
-
gamma amino butyric acid
- IC :
-
inferior colliculus
- LSO :
-
lateral superior olive
- Str :
-
strychnine
References
Adams JC, Mugnaini E (1984) Dorsal nucleus of the lateral lemniscus: A nucleus of GABAergic projection neurons. Brain Res Bull 13:585–590
Aitkin LM (1986) The auditory midbrain. Humana Press, Clifton NJ
Caird D (1991) Processing in the colliculi. In: Altschuler RA et al. (eds) Neurobiology of hearing: The central auditory system. Raven Press, New York, pp 253–292
Caspary DM (1990) Electrophysiological studies of glycinergic mechanisms in auditory brain stem structures. In: Ottersen OP, Storm-Mathiesen J (eds) Glycine neurotransmission. John Wiley & Sons, Chichester New York Brisbane Toronto Singapore, pp 391–417
Caspary DM, Havey DC, Faingold CL (1979) Effects of microiontophoretically applied glycine and GABA on neuronal response patterns in the cochlear nuclei. Brain Res 172:179–185
Casseday JH, Covey E, Vater M (1988) Connections of the superior olivary complex in the rufous horseshoe bat Rhinolophus rouxi. J Comp Neurol 278:313–329
Covey E, Vater M, Casseday JH (1991) Binaural properties of single units in the superior olivary complex of the mustache bat. J Neurophysiol 66:1080–1094
Faingold CL, Gehlbach G, Caspary DM (1989) On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons: iontophoretic studies. Brain Res 500:302–312
Faingold CL, Gehlbach G, Caspary DM (1991) Functional neuropharmacology of inferior collicullus neurons. In: Altschuler RA et al. (eds) Neurobiology of hearing: The central auditory system. Raven Press, New York, pp 223–251
Feng AS, Vater M (1985) Functional organization of the cochlear nucleus of rufous horseshoe bats (Rhinolophus rouxi): frequencies and internal connections are arranged in slabs. J Comp Neurol 235:529–553
Grothe B (1990) Versuch einer Definition des medialen Kerns des oberen Olivenkomplexes bei der Neuweltfledermaus Pteronotus pamellii. Dissertation, Ludwig Maximillian Universität, München
Grothe B, Vater M, Casseday JH, Covey E (1992) Monaural interaction of excitation and inhibiton in the medial superior olive of the mustached bat: An adaptation for biosonar. Proc Natl Acad Sci USA 89:5108–5112
Havey DC, Caspary DM (1980) A simple technique for constructing “piggy-back” multibarrel microelectrodes. Electroencephal Clin Neurophysiol 48:249–251
Irvine DRF (1986) The auditory brainstem. Progr in Sensory Physiology 7. Springer, Berlin Heidelberg New York
Kössl M, Vater M (1989) Noradrenalin enhances temporal auditory contrast and neuronal timing precision in the cochlear nucleus of the mustached bat. J Neurosci 9:4169–4178
Metzner W, Radtke-Schuller S (1987) The nuclei of the lateral lemniscus in the rufous horseshoe bat, Rhinolophus rouxi. J Comp Neurol 160:395–411
Möller J (1978) Response characteristics of inferior colliculus neurons of the awake CF-FM bat Rhinolophus ferrumequinum. II. Two-tone stimulation. J Comp Physiol 125:227–236
Möller J, Neuweiler G, Zöller H (1978) Response characteristics of inferior colliculus neurons of the awake CF-FM bat, Rhinolophus ferrumequinum. I. Single tone stimulation. J Comp Physiol 125:221–225
Moore JK, Moore RY (1987) Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat. J Comp Neurol 260:157–174
Müller CM, Scheich H (1987) GABAergic inhibition increases the neuronal selectivity to natural sounds in the avian auditory forebrain. Brain Res 414:376–380
Neuweiler G (1990) Auditory adaptations for prey capture in echolocating bats. Physiol Rev 70:615–641
Neuweiler G, Vater M (1977) Response patterns to pure tones of cochlear nucleus units in the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol 115:119–133
Oliver DL, Shneiderman A (1991) The anatomy of the inferior colliculus: A cellular basis for integration of monaural and binaural information. In: Altschuler RA et al. (eds) Neurobiology of hearing: The central auditory system. Raven Press, New York, pp 195–222
Park TJ, Pollak GD (1992) The role of GABA in shaping binaural properties and receptive fields of E/I neurons in the inferior colliculus. Abstr 18th midwinter meeting of the ARO, p 237
Pollak GD (1988) Time is traded for intensity in the bat's auditory system. Hearing Res 36:107–124
Pollak GD, Casseday JH (1989) The neural basis of echolocation in bats. Springer, Berlin Heidelberg New York London Paris Tokyo
Pollak GD, Park TJ (1992) The role of GABA in shaping monaural response properties of neurons in the inferior colliculus. Abstr 18th midwintermeeting of the ARO, p 236
Pollak GD, Schuller G (1981) Tonotopic organization and encoding features of single units in inferior colliculus of horseshoe bats: Functional implications for prey identification. J Neurophysiol 45:208–226
Rübsamen R, Neuweiler G, Sripathi K (1988) Comparative collicular tonotopy in two bat species adapted to movement detection, Hipposideros speoris and Megaderma lyra. J Comp Physiol A 163:271–285
Saint Marie RL, Ostapoff EM, Morest DK, Wenthold RJ (1989) Glycine-immunopositive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J Comp Neurol 279:382–396.
Schlegel P (1977a) Directional coding by binaural brainstem units of the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol 118:327–352.
Schlegel P (1977b) Calibrated earphones for the echolocating bat, Rhinolophus ferrumequinum. J Comp Physiol 118:353–356
Schmidt U, Schlegel P, Schweizer H, Neuweiler G (1991) Audition in vampire bats, Desmodus rotundus. J Comp Physiol A 168:45–51
Schweizer H (1981) The connections of the inferior colliculus and the organization of the brainstem auditory system in the Greater horseshoe bat (Rhinolophus ferrumequinum). J Comp Neurol 270:25–49
Shneiderman A, Oliver DL, Henkel CK (1988) Connections of the dorsal nucleus of the lateral lemniscus: An inhibitory parallel pathway in the ascending auditory system? J Comp Neurol 276:188–20
Stone TW (1985) Microiontophoresis and pressure injection. IBRO Hdb Series: Methods in the neurosciences, Vol 8. John Wiley & Sons, Chichester New York
Suga N (1964) Single unit activity in cochlear nucleus and inferior colliculus of echo-locating bats. J Physiol (Lond) 162:449–474
Suga N (1969) Classification of inferior colliculus neurons of bats in terms of responses to pure tones, FM sounds and noise bursts. J Physiol (Lond) 200:555–574
Suga N (1989) Principles of auditory information-processing derived from neuroethology. J Exp Biol 146:277–286
Suga N, Schlegel P (1973) Coding and processing in the auditory systems of FM-signal-producing bats. J Acoust Soc Am 54:174–190
Vater M, Schlegel P, Zöller H (1979) Comparative auditory neurophysiology of the inferior colliculus of two molossid bats, Molossus ater and Molossus molossus. J Comp Physiol 131:137–145
Vater M, Feng AS (1990) The functional organization of ascending and descending connections of the cochlear nucleus of horseshoe bats. J Comp Neurol 292:373–395
Vater M, Feng AS, Betz M (1985) An HRP-study of the frequency place map of the horseshoe bat cochlea: Morphological correlates of the sharp tuning to a narrow frequency band. J Comp Physiol A 157:671–686
Vater M, Kössl M, Horn A (1990a) Differential distribution of GABA and glycine in the ascending auditory pathway of horseshoe bats. In: Elsner N, Roth G (eds) Brain-Perception-Cognition. (Proc 18th Göttingen Neurobiol Conf) G Thieme, Stuttgart New York, p 142
Vater M, Kössl M, Grothe B (1990b) Physiological effects of GABA and glycine in the inferior colliculus of horseshoe bats. In: Elsner N, Roth G (eds) Brain-Perception-Cognition. (Proc 18th Göttingen Neurobiol Conf) G Thieme, Stuttgart New York, p 143
Vater M, Kössl M, Horn AKE (1992a) Immunocytochemical aspects of the functional organization of the horseshoe bat's cochlear nucleus. In: Ainsworth WA, Evans EF, Hackney CM(eds) Cochlear nucleus: Structure and function in relation to modelling. Advances in speech, hearing and language processing. Vol. III. JAI Press Ltd, London (in press)
Vater M, Kössl M, Horn AKE (1992b) GAD- and GABAimmunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J Comp Neurol (in press)
Wenstrup JJ, Ross LS, Pollak GD (1986) Binaural response organization within a frequency band representation of the inferior colliculus: Implications for sound localization. J Neurosci 6:962–973
Wenthold RJ, Hunter C (1990) Immunocytochemistry of glycine and glycine receptors in the central auditory system. In: Ottersen OP, Storm-Mathiesen J (eds) Glycine neurotransmission. John Wiley & Sons, Chichester New York Brisbane Toronto Singapore, pp 391–417
Yang LC, Pollak GD (1992) The role of GABA in sharpening tuning curves in the mustache bat's inferior colliculus. Abstr 18th midwinter meeting of the ARO, p 190
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Vater, M., Habbicht, H., Kössl, M. et al. The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J Comp Physiol A 171, 541–553 (1992). https://doi.org/10.1007/BF00194587
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DOI: https://doi.org/10.1007/BF00194587