Journal of Comparative Physiology A

, Volume 191, Issue 6, pp 535–546

Serotonin modulates responses to species-specific vocalizations in the inferior colliculus

Original Paper

Abstract

Neuromodulators such as serotonin are capable of altering the neural processing of stimuli across many sensory modalities. In the inferior colliculus, a major midbrain auditory gateway, serotonin alters the way that individual neurons respond to simple tone bursts and linear frequency modulated sweeps. The effects of serotonin are complex, and vary among neurons. How serotonin transforms the responses to spectrotemporally complex sounds of the type normally heard in natural settings has been poorly examined. To explore this issue further, the effects of iontophoretically applied serotonin on the responses of individual inferior colliculus neurons to a variety of recorded species-specific vocalizations were examined. These experiments were performed in the Mexican free-tailed bat, a species that uses a rich repertoire of vocalizations for the purposes of communication as well as echolocation. Serotonin frequently changed the number of recorded calls that were capable of evoking a response from individual neurons, sometimes increasing (15% of serotonin-responsive neurons), but usually decreasing (62% of serotonin-responsive neurons), this number. A functional consequence of these serotonin-evoked changes would be to change the population response to species-specific vocalizations.

Keywords

Serotonin Inferior colliculus Free-tailed bat Vocalization Neuromodulator 

Abbreviations

IC

Inferior colliculus

References

  1. Adams J (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538Google Scholar
  2. Aitkin L (1986) The auditory midbrain: structure and function in the central auditory pathway. Humana Press, CliftonGoogle Scholar
  3. Andersen R, Snyder R, Merzenich M (1980) The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical fields of the cat. J Comp Neurol 191:479–494Google Scholar
  4. Balcombe J, McCracken G (1992) Vocal recognition in Mexican free-tailed bats: do pups recognize mothers? Anim Behav 43:79–87Google Scholar
  5. Bauer E, Klug A, Pollak G (2002) Spectral determination of responses to species-specific calls in the dorsal nucleus of the lateral lemniscus. J Neurophysiol 88:1955–1967Google Scholar
  6. Beyerl B (1978) Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Res 145:209–223Google Scholar
  7. Bodenhamer R, Pollak G, Marsh D (1979) Coding of fine frequency information by echoranging neurons in the inferior colliculus of the Mexican free-tailed bat. Brain Res 171:530–535Google Scholar
  8. Brunso-Bechtold J, Thompson G, Masterton R (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197:705–722Google Scholar
  9. Bunin M, Wightman R (1998) Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J Neurosci 18:4854–4860Google Scholar
  10. Castro-Alamancos M (2002) Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J Neurosci 22:9651–9655Google Scholar
  11. Devilbiss D, Waterhouse B (2000) Norepinephrine exhibits two distinct profiles of action on sensory cortical neuron responses to excitatory synaptic stimuli. Synapse 37:273–282CrossRefGoogle Scholar
  12. Devilbiss D, Waterhouse B (2002) Determination and quantification of pharmacological, physiological, or behavioral manipulations on ensembles of simultaneously recorded neurons in functionally related neural circuits. J Neurosci Methods 121:181–198Google Scholar
  13. Ebert U, Ostwald J (1992) Serotonin modulates auditory information processing in the cochlear nucleus of the rat. Neurosci Lett 145:51–54Google Scholar
  14. French B, Lollar A (1998) Observations on the reproductive behavior of captive Tadarida brasileinsis mexicana (Chiroptera: Molossidae). Southw Natural 43:484–490Google Scholar
  15. French B, Lollar A (2000) Communication among Mexican free-tailed bats. Bats: Bat Conserv Internat 18:1–4Google Scholar
  16. Gelfand D, McCracken G (1986) Individual variation in the isolation calls of Mexican free-tailed bat pups (Tadarida brasiliensis mexicana). Anim Behav 34:1078–1086Google Scholar
  17. Grothe B, Schweizer H, Pollak G, Schuller G, Rosemann C (1994) Anatomy and projection patterns of the superior olivary complex in the Mexican free-tailed bat, Tadarida brasiliensis mexicana. J Comp Neurol 343:630–646Google Scholar
  18. Grothe B, Park T, Schuller G (1997) Medial superior olive in the free-tailed bat: response to pure tones and amplitude-modulated tones. J Neurophysiol 77:1553–1565Google Scholar
  19. Havey D, Caspary D (1980) A simple technique for constructing ‘piggy-back’ multibarrel microelectrodes. Electroencephalogr Clin Neurophysiol 48:249–251Google Scholar
  20. Henderson Z, Sherriff F (1991) Distribution of choline acetyltransferase immunoreactive axons and terminals in the rat and ferret brainstem. J Comp Neurol 314:147–163PubMedGoogle Scholar
  21. Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103–122Google Scholar
  22. Hoyer D, Hannon J, Martin G (2002) Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71:533–554CrossRefPubMedGoogle Scholar
  23. Hurley L, Pollak G (1999) Serotonin differentially modulates responses to tones and frequency-modulated sweeps in the inferior colliculus. J Neurosci 19:8071–8082Google Scholar
  24. Hurley L, Pollak G (2001) Serotonin effects on frequency tuning of inferior colliculus neurons. J Neurophysiol 85:828–842Google Scholar
  25. Hurley L, Pollak G (2002) Serotonin effects on latencies of inferior colliculus neurons. SFN Abstr 32:762.9Google Scholar
  26. Hurley L, Thompson A (2001) Serotonergic innervation of the auditory brainstem of the Mexican free-tailed bat, Tadarida brasiliensis. J Comp Neurol 435:78–88Google Scholar
  27. Hurley L, Thompson A, Pollak G (2002a) Serotonin in the inferior colliculus. Hear Res 168:1–11Google Scholar
  28. Hurley L, Devilbiss D, Waterhouse B (2004) A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr Opin Neurobiol 14:488–495Google Scholar
  29. Kaiser A, Covey E (1997) 5-HT innervation of the auditory pathway in birds and bats. In: Syka J (ed) Acoustical signal processing in the central auditory system. Plenum, New York, pp 71–78Google Scholar
  30. Klepper A, Herbert H (1991) Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Res 557:190–201Google Scholar
  31. Klug A, Bauer E, Hanson J, Hurley L, Meitzen J, Pollak G (2002) Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J Neurophysiol 88:1941–1954Google Scholar
  32. Kössl M, Vater M (1989) Noradrenaline enhances temporal auditory contrast and neuronal timing precision in the cochlear nucleus of the mustached bat. J Neurosci 9:4169–4178Google Scholar
  33. Linster C, Cleland T (2002) Cholinergic modulation of sensory representations in the olfactory bulb. Neural Netw 15:709–717Google Scholar
  34. Luethke L, Krubitzer L, Kaas J (1989) Connections of primary auditory cortex in the New World monkey, Saguinus. J Comp Neurol 285:487–513PubMedGoogle Scholar
  35. Manunta Y, Edeline J (1999) Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. Eur J Neurosci 11:2134–2150Google Scholar
  36. Melo L, Brandao M (1995) Role of 5-HT1A and 5-HT2 receptors in the aversion induced by electrical stimulation of inferior colliculus. Pharmacol Biochem Behav 51:317–321Google Scholar
  37. Olazábal U, Moore J (1989) Nigrotectal projection to the inferior colliculus: horseradish peroxidase transport and tyrosine hydroxylase immunohistochemical studies in rats, cats, and bats. J Comp Neurol 282:98–118Google Scholar
  38. Oliver D, Huerta M (1992) Inferior and superior colliculi. In: Webster D, Popper A (eds) The Mammalian Auditory Pathway: Neuroanatomy. Springer, Berlin Heidelberg New York, pp 168–222Google Scholar
  39. Park T, Grothe B, Pollak G, Schuller G, Koch U (1996) Neural delays shape selectivity to interaural intensity differences in the lateral superior olive. J Neurosci 16:6554–6566Google Scholar
  40. Park T, Klug A, Oswald J, Grothe B (1998) A novel circuit in the bat’s midbrain recruits neurons into sound localization processing. Naturwissenschaften 85:176–179Google Scholar
  41. Peruzzi D, Dut A (2004) GABA, serotonin and serotonin receptors in the rat inferior colliculus. Brain Res 998:247–250Google Scholar
  42. Pollak G, Marsh D, Bodenhamer R, Souther A (1977) Characteristics of phasic on neurons in inferior colliculus of unanesthetized bats with observations relating to mechanisms for echo ranging. J Neurophysiol 40:926–942Google Scholar
  43. Pollak G, Klug A, Bauer E (2003) Processing and representation of species-specific communication calls in the auditory system of bats. Int Rev Neurobiol 56:83–121Google Scholar
  44. Rasmussen K, Strecker R, Jacobs B (1986) Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli. Brain Res 369:336–340Google Scholar
  45. Ross L, Pollak G, Zook J (1988) Origin of ascending projections to an isofrequency region of the mustache bat’s inferior colliculus. J Comp Neurol 270:488–505Google Scholar
  46. Roth G, Aitkin L, Andersen R, Merzenich M (1978) Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182:661–680Google Scholar
  47. Schmidt S, Thaller J (1994) Temporal auditory summation in the echolocating bat, Tadarida brasiliensis. Hear Res 77:125–134Google Scholar
  48. Schuller G (1997) A cheap earphone for small animals with good frequency response in the ultrasonic frequency range. J Neurosci Methods 71:187–190Google Scholar
  49. Schuller G, Radtke-Schuller S, Betz M (1986) A stereotaxic method for small animals using experimentally determined reference profiles. J Neurosci Methods 18:339–350Google Scholar
  50. Simmons J, Lavender W, Lavender B, Childs J, Hulebak K, Rigden M, Sherman J, Woolman B, O’Farrell M (1978) Echolocation by free-tailed bats (Tadarida). J Comp Physiol 125:291–299Google Scholar
  51. Simmons J, Fenton M, O’Farrell M (1979) Echolocation and pursuit of prey by bats. Science 203:16–21Google Scholar
  52. Steinbusch H (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557–618Google Scholar
  53. Suta D, Kvasnak E, Popelar J, Syka J (2003) Representation of species-specific vocalizations in the inferior colliculus of the guinea pig. J Neurophysiol 90:3794–3808Google Scholar
  54. Thompson A, Hurley L (2004) Dense serotonergic innervation of principal nuclei of the superior olivary complex in mouse. Neurosci Lett 356:179–182Google Scholar
  55. Thompson G, Thompson A, Garrett K, Britton B (1994) Serotonin and serotonin receptors in the central auditory system. Otolaryngol Head Neck Surg 110:93–102Google Scholar
  56. Thompson A, Moore K, Thompson G (1995) Distribution and origin of serotoninergic afferents to guinea pig cochlear nucleus. J Comp Neurol 351:104–116Google Scholar
  57. Trulson M (1985) Simultaneous recording of dorsal raphe unit activity and serotonin release in the striatum using voltammetry in awake, behaving cats. Life Sci 37:2199–2204Google Scholar
  58. Trulson M, Jacobs B (1979) Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res 163:135–150Google Scholar
  59. Trulson M, Trulson V (1982) Differential effects of phasic auditory and visual stimuli on serotonergic neurons in the nucleus raphe dorsalis and nucleus raphe pallidus in freely moving cats. Neurosci Lett 32:137–142Google Scholar
  60. Vater M, Kössl M, Horn A (1992) GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J Comp Neurol 325:183–206PubMedGoogle Scholar
  61. Wang X, Kadia S (2001) Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. J Neurophysiol 86:2616–2620Google Scholar
  62. Wang X, Robertson D (1997) Effects of bioamines and peptides on neurones in the ventral nucleus of trapezoid body and rostral periolivary regions of the rat superior olivary complex: an in vitro investigation. Hear Res 106:20–28Google Scholar
  63. Winer J, Larue D, Diehl J, Hefti B (1998) Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400:147–174Google Scholar
  64. Zook J, Casseday J (1982) Origin of ascending projections to inferior colliculus in the mustache bat, Pteronotus parnellii. J Comp Neurol 207:14–28Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Jordan Hall/ Biology DepartmentIndiana UniversityBloomingtonUSA
  2. 2.University of TexasAustinUSA

Personalised recommendations