Journal of Comparative Physiology A

, Volume 205, Issue 2, pp 239–252 | Cite as

Evoked potential study of the inferior collicular response to constant frequency-frequency modulation (CF-FM) sounds in FM and CF-FM bats

  • Ziying Fu
  • Na Xu
  • Guimin Zhang
  • Dandan Zhou
  • Long Liu
  • Jia Tang
  • Philip Hung-Sun JenEmail author
  • Qicai ChenEmail author
Original Paper


The auditory system of echolocating bats is adapted for processing species-specific ultrasonic signals. While FM (frequency modulation) bats are strictly sensitive to the frequency ranges of their orientation signals or prey-generated noise, CF-FM (constant frequency-FM) bats have a disproportionate number of neurons tuned to frequencies near the CF component of their orientation sounds, and most of them are on–off responders. Furthermore, the inferior collicular neurons of the CF-FM bats discharged as single-on or double-on responders to CF-FM stimuli. To further study the differences in auditory signal processing of these two types of bats, as the first step we conducted an evoked potential response study in the inferior colliculus of the CF-FM bat, Hipposideros pratti and the FM bat, Pipistrellus abramus using CF, FM and CF-FM stimuli. The results showed that the CF sounds always evoked collicular on- and off-responses in CF-FM bats, but the FM bats only had on-responses to both CF and FM sounds, indicting species-specific neural circuits. However, when stimulated with CF-FM sounds, collicular responses were evoked by both the CF and FM components from both FM and CF-FM bats, suggesting they have some generic neural circuit.


CF-FM bat FM bat Inferior colliculus Auditory signal processing Evoked potential 



Best frequency


Constant frequency


Cochlear microphonic




Fast Fourier transformation


Frequency modulation




Inferior colliculus


Primary auditory neurons


Nuclei of lateral


Off-responses evoked by the CF sound


On-responses evoked by the CF sound


The responses evoked by the FM sound


The responses evoked by the CF-FM harmonic


Summated response





The experiments were conducted with the approval of the Institutional Animal Care and Use Committee of the Central China Normal University, Wuhan, Hubei, PRC. We thank the anonymous reviewers for their helpful comments on an earlier version of this manuscript. We also thank Zhongdan Cui for critically reading the manuscript. This work was supported by grants from the National Natural Science Foundation of China (#31200832 to ZF, 31571232 to QC and 31772454 to JT).

Author contributions

QC, PJ and ZF conceived and supervised the project; PJ, ZF and QC wrote the manuscript with drafts and input from the other authors; NX, ZF, GZ, DZ, LL, and JT performed the experiments and analyzed the data; ZF and QC designed the experiments.


  1. Boku S, Riquimaroux H, Simmons AM, Simmons JA (2015) Auditory brainstem response of the Japanese house bat (Pipistrellus abramus). J Acoust Soc Am 137(3):1063–1068. Google Scholar
  2. Casseday JH, Covey E (1996) A neuroethological theory of the operation of the inferior colliculus. Brain Behav Evol 47(6):323–336. Google Scholar
  3. Chaverri G, Ancillotto L, Russo D (2018) Social communication in bats. Biol Rev 93(4):1938–1954. Google Scholar
  4. Corcoran AJ, Moss CF (2017) Sensing in a noisy world: lessons from auditory specialists, echolocating bats. J Exp Biol 220(Pt 24):4554–4566. Google Scholar
  5. Feng J, Li Z, Chen M, Zhou J, Zhao H, Zhang S (2002) The echolocation comparison and the differentiation of ecology niche of five species bats live in one cave. Acta Ecol Sin 22(2):150–155. (in Chinese with English abstract) Google Scholar
  6. Fishman YI, Steinschneider M (2009) Temporally dynamic frequency tuning of population responses in monkey primary auditory cortex. Hear Res 254(1–2):64–76. Google Scholar
  7. Fitzpatrick DC, Kanwal JS, Butman JA, Suga N (1993) Combination-sensitive neurons in the primary auditory cortex of the mustached bat. J Neurosci 13: 931–940. Google Scholar
  8. Fu ZY, Tang J, Jen PHS, Chen QC (2010) The auditory response properties of single-on and double-on responders in the inferior colliculus of the leaf-nosed bat, Hipposideros armiger. Brain Res 1306: 39–52. Google Scholar
  9. Fu ZY, Tang J, Li Y, Zeng H, Chen QC (2011) Frequency-modulation component of the mimic echolocation sound can increase the sensitivity of inferior collicular neurons to sound amplitude in the leaf-nosed bat, Hipposideros armiger. Zool Stud 50(5):537–545.
  10. Fu ZY, Mei HX, Cheng L, Bai J, Tang J, Jen PHS, Chen QC (2013) Local neuronal circuits that may shape the discharge patterns of inferior collicular neurons. Neurosci Bull 29(5):541–552. Google Scholar
  11. Fu ZY, Xu N, Wang J, Tang J, Jen PHS, Chen QC (2014) The role of the FM component in shaping the number of impulses and response latency of inferior collicular neurons of Hipposideros armiger elicited by CF-FM sounds. Neurosci Lett 576(1):97–101. Google Scholar
  12. Goto K, Hiryu S, Riquimaroux H (2010) Frequency tuning and latency organization of responses in the inferior colliculus of Japanese house bat, Pipistrellus abramus. J Acoust Soc Am 128 (3):1452–1459. Google Scholar
  13. Grinnell AD (1970) Comparative auditory neurophysiology of neotropical bats employing different echolocation signals. Z Vergl Physiol 68(2):117–153. Google Scholar
  14. Grinnell AD, Hagiwara S (1972) Studies of auditory neurophysiology in non-echolocating bats, and adaptations for echolocation in one genus. Rousettus Z Vergl Physiol 76(1):82–96. Google Scholar
  15. Grinnell AD (2018) Early milestones in the understanding of echolocation in bats. J Comp Physiol A 204:519–536. Google Scholar
  16. Grothe B (1994) Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. J Neurophysiol 71(2):706. Google Scholar
  17. He J, Hashikawa T, Ojima H, Kinouchi Y (1997) Temporal integration and duration tuning in the dorsal zone of cat auditory cortex. J Neurosci 17(7):2615–2625. Google Scholar
  18. He J (2001) On and off pathways segregated at the auditory thalamus of the guinea pig. J Neurosci 21(21):8672–8679. Google Scholar
  19. Hiryu S, Hagino T, Riquimaroux H, Watanabe Y (2007) Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone. J Acoust Soc Am 121(3):1749–1757. Google Scholar
  20. Hiryu S, Hagino T, Fujioka E, Riquimaroux H, Watanabe Y (2008) Adaptive echolocation sounds of insectivorous bats, Pipistrellus abramus, during foraging flights in the field. J Acoust Soc Am 124(2):EL51–E56. Google Scholar
  21. Hsiao CJ, Jen PH. Wu CH (2015) The cochlear size of bats and rodents derived from MRI images and histology. NeuroReport 26(8):478–482. Google Scholar
  22. Jen PHS, Schlegel PA (1982) Auditory physiological properties of the neurones in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol A 147:351–363. Google Scholar
  23. Jen PHS, Suthers RA (1982) Responses of inferior collicular neurones to acoustic stimuli in certain FM and CF-FM paleotropical bats. J Comp Physiol A 146(4):423–434. Google Scholar
  24. Kanwal JS (2018) Ultrasonic social communication in bats: signal complexity and its neural management. Handbook Behav Neurosci 25:493–508. Google Scholar
  25. Kober R, Schnitzler HU (1990) Information in sonar echoes of fluttering insects available for echolocating bats. J Acoust Soc Am 87(2):882–896. Google Scholar
  26. Kopp-Scheinpflug C, Tozer AJ, Robinson SW, Tempel BL, Hennig MH, Forsythe ID (2011) The sound of silence: ionic mechanisms encoding sound termination. Neuron 71(5):911–925. Google Scholar
  27. Li YL, Fu ZY, Yang MJ, Wang J, Peng K, Yang LJ, Tang J, Chen QC (2015) Post-spike hyperpolarization participates in the formation of auditory behavior-related response patterns of inferior collicular neurons in Hipposideros pratti. Neuroscience 289:443–451. Google Scholar
  28. Liu Y, Feng J, Metzner W (2013) Different auditory feedback control for echolocation and communication in horseshoe bats. PLoS One 8(4):e62710. Google Scholar
  29. Luo F, Ma J, Li AA, Wu FJ, Chen QC, Zhang SY (2007) Echolocation calls and neurophysiological correlations with auditory response properties in the inferior colliculus of Pipistrellus abramus (Microchiroptera: Vespertilionidae). Zool Stud 46(5):622–630.
  30. Luo F, Metzner W, Wu FJ, Zhang SY, Chen QC (2008) Duration-sensitive neurons in the inferior colliculus of horseshoe bats: adaptations for using CF-FM echolocation pulses. J Neurophysiol 99(1):284–296. Google Scholar
  31. Luo J, Macias S, Ness TV, Einevoll GT, Zhang K, Moss CF (2018) Neural timing of stimulus events with microsecond precision. PLoS Biol 16(10):e2006422. Google Scholar
  32. Ma J, Metzner W, Liang B, Zhang LB, Zhang JS, Zhang SY, Shen JX (2004) Differences in diet and echolocation in four sympatric bat species and their respective ecological niches. Curr Zool 50(2):145–150. (in Chinese with English abstract)
  33. Macias S, Hechavarría JC, Kössl M, Mora EC (2013) Neurons in the inferior colliculus of the mustached bat are tuned both to echo-delay and sound duration. Neuroreport 24(8):404–409. Google Scholar
  34. Macias S, Luo J, Moss CF (2018) Natural echolocation sequences evoke echo-delay selectivity in the auditory midbrain of the FM bat, Eptesicus fuscus. J Neurophysiol. Google Scholar
  35. Neuweiler G (2003) Evolutionary aspects of bat echolocation. J Comp Physiol A 189(4):245–256. Google Scholar
  36. Park TJ, Pollak GD (1993) GABA shapes a topographic organization of response latency in the mustache bat’s inferior colliculus. J Neurosci 13(12):5172–5187. Google Scholar
  37. Pelleg-Toiba R, Wollberg Z (1989) Tuning properties of auditory cortex cells in the awake squirrel monkey. Exp Brain Res 74(2):353–364. Google Scholar
  38. Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. J Zool Lond 261(1):21–33. Google Scholar
  39. Ramprashad F, Landolt JP, Money KE, Clark D, Laufer J (1979) A morphometric study of the cochlea of the little brown bat (Myotis lucifugus). J Morphol 160(3):345–358. Google Scholar
  40. Razak KA (2018) Adaptations for substrate gleaning in bats: the pallid bat as a case study. Brain Behav Evol 91(2):97–108. Google Scholar
  41. Schnitzler HU, Denzinger A (2011) Auditory fovea and doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals. J Comp Physiol A 197(5):541–559. Google Scholar
  42. Schoeppler D, Schnitzler HU, Denzinger A (2018) Precise doppler shift compensation in the Hipposiderid bat, Hipposideros armiger. Sci Rep 8(1):4598. Google Scholar
  43. Scholl B, Gao X, Wehr M (2010) Nonoverlapping sets of synapses drive on responses and off responses in auditory cortex. Neuron 65(3):412–421. Google Scholar
  44. Shokei B, Hiroshi R, Andrea Megela S, Simmons JA (2015) Auditory brainstem response of the Japanese house bat (Pipistrellus abramus). J Acoust Soc Am 137(3):1063–1068. Google Scholar
  45. Spitzer MW, Semple MN (1995) Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. J Neurophysiol 73(4):1668–1690. Google Scholar
  46. Suga N, Jen PHS (1977) Further studies on the peripheral auditory system of the “CF-FM” bats specialized for fine frequency analysis of Doppler-shifted echoes. J Exp Biol 69(1):207–232.
  47. Suga N, Manabe T (1982) Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J Neurophysiol 47(2):225–255. Google Scholar
  48. Suga N, O’Neill WE (1979) Neural axis representing target range in the auditory cortex of the mustache bat. Science 206(4416):351–353. Google Scholar
  49. Suga N, Simmons JA, Shimozawa T (1974) Neurophysiological studies on echolocation systems in awake bats producing CF-FM orientation sounds. J Exp Biol 61(2):379–399.
  50. Suga N, Simmons JA, Jen PHS (1975) Peripheral specialization for fine analysis of doppler-shifted echoes in the auditory system of the “CF-FM” bat Pteronotus parnellii. J Exp Biol 63(1):161–192.
  51. Suga N, Neuweiler G, Moller J (1976) Peripheral auditory tuning for fine frequency analysis by the CF-FM bat, Rhinolophus ferrumequinum. IV. Properties of peripheral auditory neurons. J Comp Physiol 106:111–125. Google Scholar
  52. Suga N, O’Neill WE, Manabe T (1979) Harmonic-sensitive neurons in the auditory cortex of the mustache bat. Science 203(4377):270–274. Google Scholar
  53. Suga N (2018) Specialization of the auditory system for the processing of bio-sonar information in the frequency domain: Mustached bats. Hear Res 361:1–22. Google Scholar
  54. Surlykke A, Moss CF (2000) Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am 108(5):2419–2429. Google Scholar
  55. Tang J, Fu ZY, Jen PHS, Chen QC (2011) Recovery cycles of single-on and double-on neurons in the inferior colliculus of the leaf-nosed bat, Hipposideros armiger. Brain Res 138:114–126. Google Scholar
  56. Ulanovsky N, Moss CF (2008) What the bat’s voice tells the bat’s brain. Proc Natl Acad Sci 105(25):8491–8498. Google Scholar
  57. Vanderelst D, Lee YF, Geipel I, Kalko EKV, Kuo YM, Peremans H (2013) The noseleaf of Rhinolophus formosae focuses the frequency modulated (FM) component of the calls. Front Physiol 4:191. Google Scholar
  58. Wei L, Zhou S, Zhang LB, Liang B, Hong TY, Zhang SY (2006) Characteristics of echolocation calls and summer diet of three sympatric insectivorous bats species. Zool Res 27 (3): 235–241. (In Chinese with English abstract) Google Scholar
  59. 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):9469–9481. Google Scholar
  60. Xu N, Fu ZY, Chen QC (2014) The function of offset neurons in auditory information processing. Transl Neurosci 5(4):275–285. Google Scholar
  61. Yang MJ, Pen K, Wang J, Tang J, Fu ZY, Wang X, Chen QC (2018) Amplitude- and duration-sensitivity of single-on and double-on neurons to CF-FM Stimuli in inferior colliculus of Pratt’s round leaf bat (Hipposideros Pratti). J Comp Physiol A 204(7):653–6665. Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Ziying Fu
    • 1
  • Na Xu
    • 1
    • 4
  • Guimin Zhang
    • 1
  • Dandan Zhou
    • 1
  • Long Liu
    • 2
  • Jia Tang
    • 1
  • Philip Hung-Sun Jen
    • 3
    Email author
  • Qicai Chen
    • 1
    Email author
  1. 1.School of Life Sciences and Hubei Key Lab of Genetic Regulation & Integrative BiologyCentral China Normal UniversityWuhanChina
  2. 2.College of scienceNational University of Defense TechnologyChangshaChina
  3. 3.Division of Biological SciencesUniversity of MissouriColumbiaUSA
  4. 4.School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental HealthPeking UniversityBeijingChina

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