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

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.

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

“…For instance, female Hyla chrysoscelis use pulse rate to recognize mates while Hyla versicolor females use pulse duration. These species preferences are reflected in differences in selectivity of interval-counting neurons and long-interval selective neurons in the inferior colliculus (Schul and Bush, 2002;Rose et al, 2015;Hanson et al, 2016). The X. laevis inferior colliculus is also populated by auditory neurons that respond preferentially to sound pulse rate (Elliott et al, 2011) and auditory sensitivity to temporal features of sound pulses could differ in X. petersii and X. victorianus.…”

Frequency-channel dependent selectivity for temporal call characteristics in gray treefrogs, Hyla versicolor

“…These neurons, described in multiple anuran species, are only responsive to signals with a minimum number of correctly spaced sound pulses; signals containing gaps reset the process of temporal integration (Edwards et al, 2002;Rose et al, 2015). Correspondingly, we found that stimuli containing gaps were highly unattractive to females.…”

“…This component was identical to the 'typical H. versicolor' stimulus except that for every 3 pulses broadcast, 3 pulses were silenced. Temporal filters in the anuran auditory system are especially sensitive to gaps within calls, which reset the process of temporal integration (Henderson and Gerhardt, 2013;Rose et al, 2015;Schwartz et al, 2010). (5) Tone.…”

“…Finally, temporal filtering is well understood at higher levels of the nervous system in H. versicolor. Recordings in the auditory midbrain revealed neurons that are highly selective for conspecific AM patterns (Diekamp and Gerhardt, 1995;Hanson et al, 2015;Rose et al, 1985Rose et al, , 2015. Less is known about the temporal selectivity of lower levels of the auditory system, but a study of auditory-evoked potentials in the closely related H. chrysoscelis demonstrated that the auditory periphery is also involved in temporal processing (Schrode and Bee, 2015).…”

Calling site choice and its impact on call degradation and call attractiveness in the gray treefrog, Hyla versicolor

“…Such reductions in modulation depth were similar to structural changes that would yield declines in ΔV. These alterations could potentially attenuate the responses of interval-counting neurons in the auditory mid-brain of gray treefrogs (Rose et al 2015). Nevertheless, Kuczynski et al (2010) judged females fairly tolerant of drops in modulation depth, especially at lower signal amplitudes.…”