The Repertoire of Communication Calls Emitted by Bats and the Ways the Calls Are Processed in the Inferior Colliculus

  • George D. Pollak
  • Sari Andoni
  • Kirsten Bohn
  • Joshua X. Gittelman
Chapter
First Online:

Abstract

Bats have among the richest and most sophisticated repertoire of vocal communication calls of any mammalian group. In this review, we first describe the range of calls bats emit and the acoustic features that comprise their calls. Of particular importance are frequency modulations (FMs), as these are components in the vast majority of bats’ communication calls as well as the calls they emit for echolocation. We then consider the processing of communication calls in the inferior colliculus (IC). We show that neurons in the IC are selective for the various calls the bats emit and that this selectivity is shaped by inhibition. Computational studies showed that some neurons had one feature or filter characterized by its spectrotemporal receptive field (STRF) generated by spike-triggered averaging. In these cells, convolving conspecific calls with the STRF provides an accurate prediction of their responses to conspecific calls. Moreover a single linear combination of the excitatory and inhibitory fields explains their responses to the direction and velocity of FM sweeps. Most IC cells, however, had several spectrotemporal filters. In these cells, the nonlinear combination of two or more filters predicted the cell’s selectivity for FM sweeps and its responses to calls. The ways in which excitation and inhibition interacted to generate FM selectivity were also evaluated with in vivo whole-cell recordings. Those studies showed that the relative timing of excitation and inhibition had only a small influence on the amplitudes of the excitatory postsynaptic potentials (EPSPs) evoked by an FM signal. How the change in EPSP amplitude influenced discharge probability depended in large part on how close the EPSP was to spike threshold. If the EPSP amplitude is far from threshold, even timing changes of several ms would have little or no effect on spike probability. Conversely, if the EPSP amplitude is near threshold, then even a change in EPSP amplitude as small as a fraction of a millivolt could affect discharge probability and thus modulate the cell’s spiking directional selectivity. Taken together, these studies showed that neurons in the auditory midbrain encode specific spectrotemporal features of natural communication sounds by means of their selectivity to FM features present in their conspecific calls.

Keywords

Echolocating bats Communication calls Inhibition Spectrotemporal receptive fields In vivo whole-cell recordings Spike timing 
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References

  1. 1.
    Griffin DR (1986) Listening in the dark. Cornell University Press, Ithaca, NYGoogle Scholar
  2. 2.
    Behr O, von Helversen O (2004) Bat serenades-complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol 56:106–115CrossRefGoogle Scholar
  3. 3.
    Bohn KM, Schmidt-French B, Schwartz C, Smotherman M, Pollak GD (2009) Versatility and stereotypy of free-tailed bat songs. PLoS One 4(8):e6746PubMedCrossRefGoogle Scholar
  4. 4.
    Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B 265(1392):227–233CrossRefGoogle Scholar
  5. 5.
    Esser K-H (1994) Audio-vocal learning in a nonhuman mammal—the lesser spear-nosed bat Phyllostomus discolor. Neuroreport 5(14):1718–1720PubMedCrossRefGoogle Scholar
  6. 6.
    Knornschild M, Nagy M, Metz M, Mayer F, von Helversen O (2009) Complex vocal imitation during ontogeny in a bat. Biol Lett 6(2):156–159PubMedCrossRefGoogle Scholar
  7. 7.
    Knornschild M, Behr O, von Helversen O (2006) Babbling behavior in the sac-winged bat (Saccopteryx bilineata). Naturwissenschaften 93(9):451–454PubMedCrossRefGoogle Scholar
  8. 8.
    Kanwal JS (1999) Processing species-specific calls combination-sensitive neurons in an echolocating bat. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT Press, Cambridge, MA, pp 133–156Google Scholar
  9. 9.
    Esser KH, Condon CJ, Suga N, Kanwal JS (1997) Syntax processing by auditory cortical neurons in the FM-FM area of the mustached bat Pteronotus parnellii. Proc Natl Acad Sci U S A 94(25):14019–14024PubMedCrossRefGoogle Scholar
  10. 10.
    Bohn KM, Schmidt-French B, Ma ST, Pollak GD (2008) Syllable acoustics, temporal patterns, and call composition vary with behavioral context in Mexican free-tailed bats. J Acoust Soc Am 124(3):1838–1848PubMedCrossRefGoogle Scholar
  11. 11.
    Schwartz C, Tressler J, Keller H, Vanzant M, Ezell S, Smotherman M (2007) The tiny difference between foraging and communication buzzes uttered by the Mexican free-tailed bat, Tadarida brasiliensis. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193(8):853–863PubMedCrossRefGoogle Scholar
  12. 12.
    Pollak GD, Winer JA, O’Neill WE (1995) Perspectives on the functional organization of the mammalian auditory system: why bats are good models. In: Popper AN, Fay RR (eds) Hearing by bats, Springer handbook of auditory research. Springer, New York, pp 481–498CrossRefGoogle Scholar
  13. 13.
    Winer JA, Larue DT, Pollak GD (1995) GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. J Comp Neurol 355(3):317–353PubMedCrossRefGoogle Scholar
  14. 14.
    Pollak GD, Casseday JH (1986) The neural basis of echolocation in bats. Springer, New YorkGoogle Scholar
  15. 15.
    Pollak GD, Gittelman JX, Li N, Xie R (2011) Inhibitory projections from the ventral nucleus of the lateral lemniscus and superior paraolivary nucleus create directional selectivity of frequency modulations in the inferior colliculus: a comparison of bats with other mammals. Hear Res 273(1–2):134–144PubMedCrossRefGoogle Scholar
  16. 16.
    Zook JM, Winer JA, Pollak GD, Bodenhamer RD (1985) Topology of the central nucleus of the mustache bat’s inferior colliculus: correlation of single unit properties and neuronal architecture. J Comp Neurol 231(4):530–546PubMedCrossRefGoogle Scholar
  17. 17.
    Casseday JH, Fremouw T, Covey E (2002) The inferior colliculus: a hub for the central auditory system. In: Oertel D, Popper AN, Fay RR (eds) Integrative functions in the mammalian auditory pathway. Springer, New York, pp 238–318CrossRefGoogle Scholar
  18. 18.
    Oliver DL, Huerta MF (1992) Inferior and superior colliculi. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory system: neuroanatomy. Springer, New York, pp 168–221CrossRefGoogle Scholar
  19. 19.
    Pollak GD, Xie R, Gittelman JX, Andoni S, Li N (2011) The dominance of inhibition in the inferior colliculus. Hear Res 274(1–2):27–39PubMedCrossRefGoogle Scholar
  20. 20.
    Li N, Gittelman JX, Pollak GD (2010) Intracellular recordings reveal novel features of neurons that code interaural intensity disparities in the inferior colliculus. J Neurosci 30(43):14573–14584PubMedCrossRefGoogle Scholar
  21. 21.
    Fremouw T, Faure PA, Casseday JH, Covey E (2005) Duration selectivity of neurons in the inferior colliculus of the big brown bat: tolerance to changes in sound level. J Neurophysiol 94(3):1869–1878PubMedCrossRefGoogle Scholar
  22. 22.
    Sanchez JT, Gans D, Wenstrup JJ (2007) Contribution of NMDA and AMPA receptors to temporal patterning of auditory responses in the inferior colliculus. J Neurosci 27(8):1954–1963PubMedCrossRefGoogle Scholar
  23. 23.
    French B, Lollar A (2000) Communication among Mexican free-tailed bats. Bats Bat Conserv Int 18(2):1–4Google Scholar
  24. 24.
    French B, Lollar A (1998) Observations on the reproductive behavior of captive Tadarida brasiliensis mexicana (Chiroptera:Molossidae). Southwest Nat 43:484–490Google Scholar
  25. 25.
    Gelfand DL, McCracken GF (1986) Individual variation in the isolated calls of Mexican free-tailed bat pups. Anim Behav 34:1078–1086CrossRefGoogle Scholar
  26. 26.
    McCracken GF (1984) Communal nursing in Mexican free-tailed bat maternity colonies. Science 223:1090–1091PubMedCrossRefGoogle Scholar
  27. 27.
    Catchpole CK, Slater PJB (1995) Bird song: biological themes and variations. Cambridge University Press, CambridgeGoogle Scholar
  28. 28.
    Payne RS, McVay S (1971) Songs of humpback whales. Science 173(3997):585–597PubMedCrossRefGoogle Scholar
  29. 29.
    Marler P (2004) Science and birdsong: the good old days. In: Marler P, Slabbekoorn H (eds) Nature’s music: the science of birdsong. Elsevier/Academic, AmsterdamGoogle Scholar
  30. 30.
    Balaban E (1988) Bird song syntax: learned intraspecific variation is meaningful. Proc Natl Acad Sci U S A 85(10):3657–3660PubMedCrossRefGoogle Scholar
  31. 31.
    Pollak GD (2011) Discriminating among complex signals: the roles of inhibition for creating response selectivities. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197(5):625–640PubMedCrossRefGoogle Scholar
  32. 32.
    Portfors CV, Roberts PD, Jonson K (2009) Over-representation of species-specific vocalizations in the awake mouse inferior colliculus. Neuroscience 162(2):486–500PubMedCrossRefGoogle Scholar
  33. 33.
    Holmstrom L, Roberts PD, Portfors CV (2007) Responses to social vocalizations in the inferior colliculus of the mustached bat are influenced by secondary tuning curves. J Neurophysiol 98(6):3461–3472PubMedCrossRefGoogle Scholar
  34. 34.
    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(6):3794–3808PubMedCrossRefGoogle Scholar
  35. 35.
    Klug A, Bauer EE, Hanson JT, Hurley L, Meitzen J, Pollak GD (2002) Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J Neurophysiol 88(4):1941–1954PubMedGoogle Scholar
  36. 36.
    Xie R, Meitzen J, Pollak GD (2005) Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei. J Neurophysiol 94(6):4019–4037PubMedCrossRefGoogle Scholar
  37. 37.
    Andoni S, Li N, Pollak GD (2007) Spectrotemporal receptive fields in the inferior colliculus revealing selectivity for spectral motion in conspecific vocalizations. J Neurosci 27(18):4882–4893PubMedCrossRefGoogle Scholar
  38. 38.
    Portfors CV (2004) Combination sensitivity and processing of communication calls in the inferior colliculus of the Moustached bat Pteronotus parnellii. An Acad Bras Cienc 76(2):253–257PubMedCrossRefGoogle Scholar
  39. 39.
    Portfors CV, Mayko ZM, Jonson K, Cha GF, Roberts PD (2011) Spatial organization of receptive fields in the auditory midbrain of awake mouse. Neuroscience 193:429–439PubMedCrossRefGoogle Scholar
  40. 40.
    Kowalski N, Depireux DA, Shamma SA (1996) Analysis of dynamic spectra in ferret primary auditory cortex. I. Characteristics of single-unit responses to moving ripple spectra. J Neurophysiol 76(5):3503–3523PubMedGoogle Scholar
  41. 41.
    Kowalski N, Depireux DA, Shamma SA (1996) Analysis of dynamic spectra in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary dynamic spectra. J Neurophysiol 76(5):3524–3534PubMedGoogle Scholar
  42. 42.
    Klein DJ, Depireux DA, Simon JZ, Shamma SA (2000) Robust spectrotemporal reverse correlation for the auditory system: optimizing stimulus design. J Comput Neurosci 9(1):85–111PubMedCrossRefGoogle Scholar
  43. 43.
    Depireux DA, Simon JZ, Klein DJ, Shamma SA (2001) Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. J Neurophysiol 85(3):1220–1234PubMedGoogle Scholar
  44. 44.
    Escabi MA, Schreiner CE (2002) Nonlinear spectrotemporal sound analysis by neurons in the auditory midbrain. J Neurosci 22(10):4114–4131PubMedGoogle Scholar
  45. 45.
    Fuzessery ZM, Hall JC (1996) Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76(2):1059–1073PubMedGoogle Scholar
  46. 46.
    Koch U, Grothe B (1998) GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol 80(1):71–82PubMedGoogle Scholar
  47. 47.
    Casseday JH, Covey E, Grothe B (1997) Neural selectivity and tuning for sinusoidal frequency modulations in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77(3):1595–1605PubMedGoogle Scholar
  48. 48.
    Andoni S, Pollak GD (2011) Selectivity for spectral motion as a neural computation for encoding natural communication signals in bat inferior colliculus. J Neurosci 31(46):16529–16540PubMedCrossRefGoogle Scholar
  49. 49.
    Razak KA, Fuzessery ZM (2006) Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. J Neurophysiol 96(3):1303–1319PubMedCrossRefGoogle Scholar
  50. 50.
    Suga N (1965) Analysis of frequency modulated sounds by auditory neurons of echolocating bats. J Physiol 179:26–53PubMedGoogle Scholar
  51. 51.
    Voytenko SV, Galazyuk AV (2007) Intracellular recording reveals temporal integration in inferior colliculus neurons of awake bats. J Neurophysiol 97(2):1368–1378PubMedCrossRefGoogle Scholar
  52. 52.
    Xie R, Gittelman JX, Li N, Pollak GD (2008) Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience 154(1):245–256PubMedCrossRefGoogle Scholar
  53. 53.
    Rust NC, Schwartz O, Movshon JA, Simoncelli EP (2005) Spatiotemporal elements of macaque v1 receptive fields. Neuron 46(6):945–956PubMedCrossRefGoogle Scholar
  54. 54.
    Simoncelli EP, Pillow J, Paninski L, Schwartz O, Gazzaniga M (2004) Characterization of neural responses with stochastic stimuli. In: Gazzaniga M (ed) The cognitive neurosciences. MIT Press, Cambridge, MAGoogle Scholar
  55. 55.
    Woolley SM, Gill PR, Theunissen FE (2006) Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain. J Neurosci 26(9):2499–2512PubMedCrossRefGoogle Scholar
  56. 56.
    David SV, Mesgarani N, Fritz JB, Shamma SA (2009) Rapid synaptic depression explains nonlinear modulation of spectro-temporal tuning in primary auditory cortex by natural stimuli. J Neurosci 29(11):3374–3386PubMedCrossRefGoogle Scholar
  57. 57.
    Woolley SM, Casseday JH (2005) Processing of modulated sounds in the zebra finch auditory midbrain: responses to noise, frequency sweeps, and sinusoidal amplitude modulations. J Neurophysiol 94(2):1143–1157PubMedCrossRefGoogle Scholar
  58. 58.
    Gittelman JX, Li N, Pollak GD (2009) Mechanisms underlying directional selectivity for frequency modulated sweeps in the inferior colliculus revealed by in vivo whole-cell recordings. J Neurosci 29:13030–13041PubMedCrossRefGoogle Scholar
  59. 59.
    Gittelman JX, Li N (2010) FM velocity selectivity in the inferior colliculus is inherited from velocity-selective inputs and enhanced by spike threshold. J Neurophysiol 106(5):2399–2414CrossRefGoogle Scholar
  60. 60.
    Gittelman JX, Pollak GD (2011) It’s about time: how input timing is used and not used to create emergent properties in the auditory system. J Neurosci 31(7):2576–2583PubMedCrossRefGoogle Scholar
  61. 61.
    Xie R, Gittelman JX, Pollak GD (2007) Rethinking tuning: in vivo whole-cell recordings of the inferior colliculus in awake bats. J Neurosci 27(35):9469–9481PubMedCrossRefGoogle Scholar
  62. 62.
    Fuzessery ZM, Richardson MD, Coburn MS (2006) Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat. J Neurophysiol 96(3):1320–1336PubMedCrossRefGoogle Scholar
  63. 63.
    Suga N, Schlegel P (1973) Coding and processing in the auditory systems of FM-signal-producing bats. J Acoust Soc Am 54(1):174–190PubMedCrossRefGoogle Scholar
  64. 64.
    Suga N (1973) Feature extraction in the auditory system of bats. In: Moller AR (ed) Basic mechanisms in hearing. Academic, New York, pp 675–744CrossRefGoogle Scholar
  65. 65.
    Brimijoin WO, O’Neill WE (2005) On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus. Hear Res 210(1–2):63–79PubMedCrossRefGoogle Scholar
  66. 66.
    Covey E, Casseday JH (1999) Timing in the auditory system of the bat. Annu Rev Physiol 61:457–476PubMedCrossRefGoogle Scholar
  67. 67.
    Yue Q, Casseday JH, Covey E (2007) Response properties and location of neurons selective for sinusoidal frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol 98(3):1364–1373PubMedCrossRefGoogle Scholar
  68. 68.
    Ye CQ, Poo MM, Dan Y, Zhang XH (2010) Synaptic mechanisms of direction selectivity in primary auditory cortex. J Neurosci 30(5):1861–1868PubMedCrossRefGoogle Scholar
  69. 69.
    Razak KA, Fuzessery ZM (2009) GABA shapes selectivity for the rate and direction of frequency modulated sweeps in the auditory cortex. J Neurophysiol 102:1366–1378PubMedCrossRefGoogle Scholar
  70. 70.
    Zhang LI, Tan AY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424(6945):201–205PubMedCrossRefGoogle Scholar
  71. 71.
    Loftus WC, Bishop DC, Oliver DL (2010) Differential patterns of inputs create functional zones in central nucleus of inferior colliculus. J Neurosci 30(40):13396–13408PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • George D. Pollak
    • 1
  • Sari Andoni
    • 1
  • Kirsten Bohn
    • 2
  • Joshua X. Gittelman
    • 3
  1. 1.Section of Neurobiology, Center for Perceptual SystemsThe University of Texas at AustinAustinUSA
  2. 2.Florida International UniversityMiamiUSA
  3. 3.Department of ScienceWashington State UniversityVancouverUSA

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