Species-specificity of temporal processing in the auditory midbrain of gray treefrogs: interval-counting neurons
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Abstract
Interval-counting neurons (ICNs) respond after a threshold number of sound pulses have occurred with specific intervals; a single aberrant interval can reset the counting process. Female gray treefrogs, Hyla chrysoscelis and H. versicolor, discriminate against synthetic ‘calls’ possessing a single interpulse interval 2–3 three times the optimal value, suggesting that ICNs are important for call recognition. The calls of H. versicolor consist of pulses that are longer in duration, rise more slowly in amplitude and are repeated at a slower rate than those of H. chrysoscelis. Results of recordings from midbrain auditory neurons in these species include: (1) ICNs were found in both species and their temporal selectivity appeared to result from interplay between excitation and inhibition; (2) band-pass cells in H. versicolor were tuned to slower pulse rates than those in H. chrysoscelis; (3) ICNs that were selective for slow-rise pulse shape were found almost exclusively in H. versicolor, but fast-rise-selective neurons were found in both species, and (4) band-suppression ICNs in H. versicolor showed response minima at higher pulse rates than those in H. chrysoscelis. Selectivity of midbrain ICNs for pulse rise time and repetition rate thus correlate well with discriminatory abilities of these species that promote reproductive isolation.
Keywords
Whole-cell recording Anurans Rise-time selectivity Amplitude modulation Inferior colliculusAbbreviations
- ICN
Interval-counting neuron
- ICanuran
Anuran inferior colliculus
- AM
Amplitude modulation
- SAM
Sinusoidal amplitude modulation
- SPL
Sound pressure level in decibels (dB), re 2 × 10−5 N/m2
- EPSP
Excitatory postsynaptic potential
- IPSP
Inhibitory postsynaptic potential
- BEF
Best excitatory frequency
Notes
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.
References
- Alder TB, Rose GJ (1998) Long-term temporal integration in the anuran auditory system. Nat Neurosci 1:519–523CrossRefPubMedGoogle Scholar
- 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 186:923–937CrossRefPubMedGoogle Scholar
- Baker CA, Carlson BA (2014) Short-term depression, temporal summation, and onset inhibition shape interval tuning in midbrain neurons. J Neurosci 34:14272–14287CrossRefPubMedGoogle 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 63:7–14CrossRefGoogle Scholar
- Carlson BA (2009) Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. J Neurosci 29:9417–9428CrossRefPubMedCentralPubMedGoogle Scholar
- Diekamp B, Gerhardt HC (1995) Selective phonotaxis to advertisement calls in the grey treefrog Hyla versicolor: behavioral experiments and neurophysiological correlates. J Comp Physiol A 177:173–190CrossRefPubMedGoogle Scholar
- Edwards CJ, Rose GJ (2003) Interval-integration underlies amplitude modulation band-suppression selectivity in the anuran midbrain. J Comp Physiol A 189:907–914CrossRefGoogle Scholar
- Edwards CJ, Leary CJ, Rose GJ (2007) Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci 27:13384–13392CrossRefPubMedGoogle 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 100:3407–3416CrossRefPubMedCentralPubMedGoogle Scholar
- George AA, Lyons-Warren AM, Ma X, Carlson BA (2011) A diversity of synaptic filters are created by temporal summation of excitation and inhibition. J Neurosci 31:14721–14734CrossRefPubMedCentralPubMedGoogle 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 99–167Google 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 59:395–408CrossRefPubMedGoogle 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 211:2609–2616CrossRefPubMedCentralPubMedGoogle Scholar
- Gerhardt HC, Doherty JA (1988) Acoustic communication in the gray treefrog Hyla versicolor: evolutionary and neurobiological implications. J Comp Physiol A 162:261–278CrossRefGoogle 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 185:33–40CrossRefPubMedGoogle Scholar
- Henderson JJ, Gerhardt HC (2013) Restoration of call attractiveness by novel acoustic appendages in grey treefrogs. Anim Behav 86:537–543CrossRefGoogle 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–E101CrossRefPubMedGoogle Scholar
- Johnson C (1963) Additional evidence of sterility between call-types in the Hyla versicolor complex. Copeia 1963:139–143CrossRefGoogle Scholar
- Keller MJ, Gerhardt HC (2001) Polyploidy alters advertisement call structure in gray treefrogs. Proc R Soc B 268:341–345CrossRefPubMedCentralPubMedGoogle Scholar
- Leary CJ, Edwards CJ, Rose GJ (2008) Midbrain auditory neurons integrate excitation and inhibition to generate duration selectivity: an in vivo whole-cell patch study in anurans. J Neurosci 28:5481–5493CrossRefPubMedCentralPubMedGoogle Scholar
- Rose GJ (2014) Time computations in anuran auditory systems. Front Physiol 5:206CrossRefPubMedCentralPubMedGoogle Scholar
- Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog. Science 219:1087–1089CrossRefPubMedGoogle Scholar
- Rose G, Capranica RR (1984) Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters. J Comp Physiol A 154:211–219CrossRefGoogle Scholar
- Rose GJ, Capranica RR (1985) Sensitivity to amplitude modulated sounds in the anuran auditory nervous system. J Neurophysiol 53:446–465PubMedGoogle Scholar
- Rose GJ, Fortune ES (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26:89–94PubMedGoogle Scholar
- Rose GJ, Brenowitz EA, Capranica RR (1985) Species specificity and temperature dependency of temporal processing by the auditory midbrain of two species of treefrogs. J Comp Physiol A 157:763–769CrossRefPubMedGoogle Scholar
- Rose GJ, Leary CJ, Edwards CJ (2011) Interval-counting neurons in the anuran auditory midbrain: factors underlying diversity of interval tuning. J Comp Physiol A 197:97–108CrossRefGoogle Scholar
- Ryan MJ, Rand AS (1993) Sexual selection and signal evolution: the ghost of biases past. Proc R Soc B 340:187–195Google Scholar
- Schul J, Bush SL (2002) Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs. Proc R Soc B 269:1847–1852CrossRefPubMedCentralPubMedGoogle Scholar
- Schwartz JJ, Huth K, Hunce R, Lentine B (2010) Effect of anomalous pulse timing on call discrimination by females of the gray treefrog (Hyla versicolor): behavioral correlates of neurobiology. J Exp Biol 213:2066–2072CrossRefPubMedGoogle Scholar
- Seeba F, Schwartz JJ, Bee MA (2010) Testing an auditory illusion in frogs: perceptual restoration or sensory bias? Anim Behav 79:1317–1328CrossRefPubMedCentralPubMedGoogle Scholar
- Tucker MA, Gerhardt HC (2012) Parallel changes in mate-attracting calls and female preferences in autotriploid tree frogs. Proc R Soc B 279:1583–1587CrossRefPubMedCentralPubMedGoogle Scholar
- Velez A, Bee MA (2011) Dip listening and the cocktail party problem in grey treefrogs: signal recognition in temporally fluctuating noise. Anim Behav 82:1319–1327CrossRefPubMedCentralPubMedGoogle Scholar