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.
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
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
Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. The J Neurosci 20:470–484
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
Edwards CJ, Alder TB, Rose GJ (2002) Auditory midbrain neurons that count. Nat Neurosci 5:934–936
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
Edwards CJ, Leary CJ, Rose GJ (2007) Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci 27:13384–13392
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
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
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
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
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
Gerhardt HC, Doherty J (1988) Acoustic communication in the gray treefrog, Hyla versicolor: evolutionary and neurobiological implications. J Comp Physiol A 162:261–278
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
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
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
Hall JC, Feng AS (1988) Influence of envelope rise time on neural responses in the auditory system of anurans. Hear Res 36:261–276
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
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
Johnson C (1963) Additional evidence of sterility between call-types in the Hyla versicolor complex. Copeia 1963:139–143
Keller MJ, Carl Gerhardt H (2001) Polyploidy alters advertisement call structure in gray treefrogs. Proc R Soc B 268:341–345
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
Reichert MS, Gerhardt HC (2014) Behavioral strategies and signaling in interspecific aggressive interactions in gray tree frogs. Behav Ecol 25:520–530
Rose GJ (2014) Time computations in anuran auditory systems. Front Physiol 5:206
Rose GJ, Brenowitz EA (2002) Pacific treefrogs use temporal integration to differentiate advertisement from encounter calls. Anim Behav 63:1183–1190
Rose GJ, Fortune ES (1996) New techniques for making whole-cell recording from CNS neurons in vivo. Neurosci Res 26:89–94
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
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
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
Suga N (1971) Responses of inferior collicular neurones of bats to tone bursts with different rise times. J Physiol 217:159–177
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
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
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
Corresponding author
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-015-1054-z