Effect of anomalous pulse timing on call discrimination by females of the gray treefrog (Hyla versicolor): behavioral correlates of neurobiology

Abstract

SUMMARYResearch has demonstrated that certain midbrain neurons of anurans 'count' interpulse intervals (IPIs). Some neurons fire after exposure to fewer intervals than do others. Counting can be reset to zero if an IPI falls outside the cell's tolerance range. We tested female gray treefrogs for behavioral correlates of these neural response patterns using phonotaxis tests in order to gain a better understanding of the mechanistic bases of female responses to calls. For example, previous work demonstrated females often prefer longer to shorter pulsed advertisement calls, even when the former occur at lower rates. Call attractiveness can also be reduced when pulse duration and timing have been manipulated experimentally or disrupted by acoustic interference. In this study, female responses were consistent with neural data, emphasizing the importance of IPIs. Females discriminated in favor of calls with normal interpulse timing relative to those in which a single IPI was too long or too short. Our data suggest that neural resetting of interval counting by inappropriate intervals may more strongly influence females than reduced firing in response to such intervals on an individual basis. Data also suggest a transition point between 125ms and 175ms at which an interval between pulse strings is treated as an interval between calls.

Time computations in anuran auditory systems

“…Thus, stimuli in which successive pulses have intervals that are alternately shorter or longer than optimal are ineffective, and elicit primarily inhibition. Remarkably, and consistent with the behavioral results mentioned earlier (Schwartz et al, 2010), a single long interval (2–3 times optimal) that is embedded in a series of optimally timed pulses can completely reset the interval-counting process (Figure 2C). The rate-dependent enhancement of excitation, which plays a critical role in the interval selectivity and counting properties of these neurons, appears to be reset by a long interval (arrows, Figure 2C); the first pulse following the gap elicits a small EPSP and large IPSP, shifting the balance once again in favor of the inhibition.…”

“…Also, longer calls tend to be favored, even when alternatives that are atypically short in duration are repeated more often to maintain equal total stimulus energy (Klump and Gerhardt, 1987); this preference appears to saturate in the range of durations seen for calls of males in the breeding season (Ward et al, 2013). Remarkably, inserting a gap in a sequence of regularly repeated pulses can markedly reduce call attractiveness (Schwartz et al, 2010). These discriminative capacities are important in the reproductive biology of anurans, and are under the forces of natural and sexual selection.…”

Dip listening and the cocktail party problem in grey treefrogs: signal recognition in temporally fluctuating noise

“…In the eastern grey treefrog ( H. versicolor ), in which the pulses and interpulse intervals of the call are about twice as long as those of Cope’s grey treefrogs ( H. chrysoscelis ), the threshold number of pulses necessary to elicit phonotaxis is between three and six pulses (Bush et al 2002). A neurophysiological mechanism that may explain these behavioural data involves “pulse-integrator” neurons in the frog midbrain that only fire in response to a threshold number of consecutive pulses produced with specific interpulse intervals (Alder & Rose 1998; Edwards et al 2002; Schwartz et al 2010a). Importantly, different neurons can have different threshold numbers of interpulse intervals.…”

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

“…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.…”

“…Experiment 4: effects of gaps on call attractiveness Female H. versicolor discriminate against calls with missing pulses (Schwartz et al, 2010). In this experiment, we asked whether females would also discriminate against calls in which pulses were missing in only one of the two frequency channels, and whether this discrimination is frequency channel dependent.…”