Skip to main content
Log in

Species specificity of temporal processing in the auditory midbrain of gray treefrogs: long-interval neurons

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

In recently diverged gray treefrogs (Hyla chrysoscelis and H. versicolor), advertisement calls that differ primarily in pulse shape and pulse rate act as an important premating isolation mechanism. Temporally selective neurons in the anuran inferior colliculus may contribute to selective behavioral responses to these calls. Here we present in vivo extracellular and whole-cell recordings from long-interval-selective neurons (LINs) made during presentation of pulses that varied in shape and rate. Whole-cell recordings revealed that interplay between excitation and inhibition shapes long-interval selectivity. LINs in H. versicolor showed greater selectivity for slow-rise pulses, consistent with the slow-rise pulse characteristics of their calls. The steepness of pulse-rate tuning functions, but not the distributions of best pulse rates, differed between the species in a manner that depended on whether pulses had slow or fast-rise shape. When tested with stimuli representing the temporal structure of the advertisement calls of H. chrysoscelis or H. versicolor, approximately 27 % of LINs in H. versicolor responded exclusively to the latter stimulus type. The LINs of H. chrysoscelis were less selective. Encounter calls, which are produced at similar pulse rates in both species (≈5 pulses/s), are likely to be effective stimuli for the LINs of both species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alder TB, Rose GJ (2000) Integration and recovery processes contribute to the temporal selectivity of neurons in the midbrain of the northern leopard frog, Rana pipiens. J Comp Physiol A 186:923–937

    Article  PubMed  CAS  Google Scholar 

  • Bush SL, Gerhardt HC, Schul J (2002) Pattern recognition and call preferences in treefrogs (Anura: Hylidae): a quantitative analysis using a no-choice paradigm. Anim Behav 63:7–14

    Article  Google Scholar 

  • Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. The J Neurosci 20:470–484

    PubMed  CAS  Google Scholar 

  • Diekamp B, Gerhardt HC (1995) Selective phonotaxis to advertisement calls in the gray treefrog Hyla versicolor: behavioral experiments and neurophysiological correlates. J Comp Physiol A 177:173–190

    Article  PubMed  CAS  Google Scholar 

  • Edwards CJ, Alder TB, Rose GJ (2002) Auditory midbrain neurons that count. Nat Neurosci 5:934–936

    Article  PubMed  CAS  Google Scholar 

  • Edwards CJ, Alder TB, Rose GJ (2005) Pulse rise time but not duty cycle affects the temporal selectivity of neurons in the anuran midbrain that prefer slow AM rates. J Neurophysiol 93:1336–1341

    Article  PubMed  Google Scholar 

  • Edwards CJ, Leary CJ, Rose GJ (2007) Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci 27:13384–13392

    Article  PubMed  CAS  Google Scholar 

  • Edwards CJ, Leary CJ, Rose GJ (2008) Mechanisms of long-interval selectivity in midbrain auditory neurons: roles of excitation, inhibition, and plasticity. J Neurophysiol 100:3407–3416

    Article  PubMed  PubMed Central  Google Scholar 

  • Felix RA 2nd, Portfors CV (2007) Excitatory, inhibitory and facilitatory frequency response areas in the inferior colliculus of hearing impaired mice. Hear Res 228:212–229

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerhardt HC (2001) Acoustic communication in two groups of closely related treefrogs. In: Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ (eds) Advances in the study of behavior, vol 30. Academic Press, New York, pp 99–167

    Google Scholar 

  • Gerhardt HC (2005) Advertisement-call preferences in diploid-tetraploid treefrogs (Hyla chrysoscelis and Hyla versicolor): implications for mate choice and the evolution of communication systems. Evolution 59:395–408

    Article  PubMed  Google Scholar 

  • Gerhardt HC (2008) Phonotactic selectivity in two cryptic species of gray treefrogs: effects of differences in pulse rate, carrier frequency and playback level. J Exp Biol 211:2609–2616

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerhardt HC, Doherty J (1988) Acoustic communication in the gray treefrog, Hyla versicolor: evolutionary and neurobiological implications. J Comp Physiol A 162:261–278

    Article  Google Scholar 

  • Gerhardt HC, Schul J (1999) A quantitative analysis of behavioral selectivity for pulse rise-time in the gray treefrog, Hyla versicolor. J Comp Physiol A 185:33–40

    Article  PubMed  CAS  Google Scholar 

  • Gooler DM, Feng AS (1992) Temporal coding in the frog auditory midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli. J Neurophysiol 67:1–22

    PubMed  CAS  Google Scholar 

  • Gordon M, O’Neill WE (1998) Temporal processing across frequency channels by FM selective auditory neurons can account for FM rate selectivity. Hear Res 122:97–108

    Article  PubMed  CAS  Google Scholar 

  • Hall JC, Feng AS (1988) Influence of envelope rise time on neural responses in the auditory system of anurans. Hear Res 36:261–276

    Article  PubMed  CAS  Google Scholar 

  • Holloway AK, Cannatella DC, Gerhardt HC, Hillis DM (2006) Polyploids with different origins and ancestors form a single sexual polyploid species. Am Nat 167:E88–E101

    Article  PubMed  Google Scholar 

  • Jagadeesh B, Wheat HS, Ferster D (1993) Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex. Science 262:1901–1904

    Article  PubMed  CAS  Google Scholar 

  • Johnson C (1963) Additional evidence of sterility between call-types in the Hyla versicolor complex. Copeia 1963:139–143

    Article  Google Scholar 

  • Keller MJ, Carl Gerhardt H (2001) Polyploidy alters advertisement call structure in gray treefrogs. Proc R Soc B 268:341–345

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kruse KC (1981) Phonotactic responses of female northern leopard frogs (Rana pipiens) to Rana blairi, a presumed hybrid, and conspecific mating trills. J Herpetol 15(2):145–150

    Article  Google Scholar 

  • Reichert MS, Gerhardt HC (2014) Behavioral strategies and signaling in interspecific aggressive interactions in gray tree frogs. Behav Ecol 25:520–530

    Article  Google Scholar 

  • Rose GJ (2014) Time computations in anuran auditory systems. Front Physiol 5:206

    Article  PubMed  PubMed Central  Google Scholar 

  • Rose GJ, Brenowitz EA (2002) Pacific treefrogs use temporal integration to differentiate advertisement from encounter calls. Anim Behav 63:1183–1190

    Article  Google Scholar 

  • Rose GJ, Fortune ES (1996) New techniques for making whole-cell recording from CNS neurons in vivo. Neurosci Res 26:89–94

    PubMed  CAS  Google Scholar 

  • Rose GJ, Brenowitz EA, Capranica R (1985) Species specificity and temperature dependency of temporal processing by the auditory midbrain of two species of treefrogs. J Comp Physiol A 157:763–769

    Article  PubMed  CAS  Google Scholar 

  • Rose GJ, Hanson JL, Leary CJ, Graham JA, Alluri RK, Vasquez-Opazo GA (2015) Species-specificity of temporal processing in the auditory midbrain of gray treefrogs: interval-counting neurons. J Comp Physiol A 201(5):485–503

    Article  Google Scholar 

  • Schul J, Bush SL (2002) Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs. Proc R Soc B 201:1847–1852

    Article  Google Scholar 

  • Suga N (1971) Responses of inferior collicular neurones of bats to tone bursts with different rise times. J Physiol 217:159–177

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tucker MA, Gerhardt HC (2011) Parallel changes in mate-attracting calls and female preferences in autotriploid tree frogs. Proc R Soc B 279:1583–1587

    Article  PubMed  PubMed Central  Google Scholar 

  • Vélez A, Bee MA (2011) Dip listening and the cocktail party problem in grey treefrogs: signal recognition in temporally fluctuating noise. Anim Behav 82:1319–1327

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank H.C. Gerhardt, J. Schwartz and their colleagues for providing the animals used in this study. We also thank Stephen Odom and Caleb Herrick for assisting in experiments and data processing. This work was supported by a grant from NIDCD. Animals were prepared for recording according to previously published methods (see Alder and Rose 2000; Rose et al. 2015).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jessica L. Hanson.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hanson, J.L., Rose, G.J., Leary, C.J. et al. Species specificity of temporal processing in the auditory midbrain of gray treefrogs: long-interval neurons. J Comp Physiol A 202, 67–79 (2016). https://doi.org/10.1007/s00359-015-1054-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-015-1054-z

Keywords

Navigation