Modified specific components of conspecific advertisement calls influence behavioral and neural responses in music frogs

Abstract

Vocal communication plays a critical role in the transfer and exchange of information among animals. However, it remains unclear how modifications to specific call components simultaneously affect behavioral and neural responses. To address these issues, we conducted phonotaxis experiments and neural signal recordings in Emei music frogs (Nidirana daunchina), exposing them to auditory stimuli with varying degrees of information coherence violations. During the electrophysiological recordings, we also presented stimuli with altered physical properties featuring rising intonation. The phonotaxis experiments showed that females exhibited reduced attraction to altered calls with potential information coherence violations, suggesting that information coherence may influence female choice. Similarly, the electrophysiological experiments indicated a correlation between the amplitudes of the N400 and late positive components (LPC) with information incongruity and altered physical properties, respectively. Notably, the N400 amplitudes increased proportionally with the extent of potential information coherence violations. Given that N400 is a well-established neural indicator for prediction error in perceptual processes, including semantic processing in humans, and considering the significant evolutionary conservation of brain structure and function among vertebrates, these findings suggest that information coherence contained in the calls plays a crucial role in anuran vocal communication.

Fig. 1. The number and latencies of female chioces.

The number and latencies of female choices for the treatment stimuli (A, B) and control stimuli (C, D) (n = 34 in each group). OC the original advertisement call with six notes, OCP the rising intonation version of OC (where the pitch of the sixth note was increased by 15%), OR the sixth note of OC was reversed in situ, OS the sixth note of OC was replaced by silence, OQ the sixth note of OC was replaced by the sixth note of an advertisement call of Quasipaa boulengeri (a sympatric anuran species), OW the sixth note of OC was replaced by white noise. The control stimuli for treatment stimuli are denoted as OCC, OCPC, ORC, OSC, OQC, and OWC respectively, where the first five notes of each treatment stimulus were reversed in situ while the sixth component remained unchanged. *p < 0.05.

Fig. 2. The average amplitudes of N400.

The average amplitudes of N400 for the control (A) and treatment (B) stimuli (n = 16 in each group). LT and RT the left and right sides of the telencephalon, LD and RD the left and right sides of the diencephalon, LM and RM the left and right sides of the mesencephalon, OC the original advertisement call with six notes, OCP the rising intonation version of OC (where the pitch of the sixth note was increased by 15%), OQ the sixth note of OC was replaced by the sixth note of an advertisement call of Quasipaa boulengeri (a sympatric anuran species), OQP the rising intonation version of OQ (where the pitch of the sixth component of OQ was increased by 15%), OW the sixth note of OC was replaced by white noise, OWP the rising intonation version of OW (where the pitch of the sixth component of OW was increased by 15%). The control stimuli for treatment stimuli are denoted as OCC, OCPC, OQC, OQPC, OWC, and OWPC, respectively, where the first five notes of each treatment stimulus were reversed in situ while the sixth component remained unchanged. *p < 0.05.

Fig. 3. The average amplitudes of the late positive component.

The average amplitudes of the late positive component for the control (A) and treatment (B) stimuli (n = 16 in each group). LT and RT the left and right sides of the telencephalon, LD and RD the left and right sides of the diencephalon, LM and RM the left and right sides of the mesencephalon, OC the original advertisement call with six notes, OCP the rising intonation version of OC (where the pitch of the sixth note was increased by 15%), OQ the sixth note of OC was replaced by the sixth note of an advertisement call of Quasipaa boulengeri (a sympatric anuran species), OQP the rising intonation version of OQ (where the pitch of the sixth component of OQ was increased by 15%), OW the sixth note of OC was replaced by white noise, OWP the rising intonation version of OW (where the pitch of the sixth component of OW was increased by 15%). The control stimuli for treatment stimuli are denoted as OCC, OCPC, OQC, OQPC, OWC, and OWPC, respectively, where the first five notes of each treatment stimulus were reversed in situ while the sixth component remained unchanged. *p < 0.05.

Fig. 4. Waveforms and spectrograms of the six treatment stimuli for phonotaxis experiments.

A represents the original advertisement call (OC), B illustrates the rising intonation version of OC, where the pitch of the sixth note was increased by 15% (OCP), C shows the modified version of OC, where the sixth note was replaced by the sixth note of an advertisement call from a sympatric anuran species, Quasipaa boulengeri (OQ), D presents a modified version of OC with the last note was reversed in situ (OR), E shows a modified version of OC with the last note replaced by silence (OS), F demonstrates the altered version of OC, with the last note replaced by white noise (OW). It is worth noting that the rising intonation in the last note (OCP) results in measurable alterations in the frequency spectrum profiles of the last components compared to the original version (OCP vs. OC).

Fig. 5. Electrode placements and 10-second samples of typical EEG tracings for each brain area.

LT and RT the left and right sides of the telencephalon, LD and RD the left and right sides of the diencephalon, LM and RM the left and right sides of the mesencephalon, C the reference electrode implanted above the cerebellum. The intersection point of the three bold dashed lines in the frog’s head represents the intersection of the suture lines.

Fig. 6. Waveforms and spectrograms of the six treatment stimuli used for electrophysiological experiments.

A represents the original advertisement call (OC), B illustrates the rising intonation version of OC, where the pitch of the sixth note was increased by 15% (OCP), C shows the modified version of OC, where the sixth note was replaced by the sixth note of an advertisement call from a sympatric anuran species, Quasipaa boulengeri (OQ), D presents the rising intonation version of OQ, with a 15% increase in the pitch of the sixth component (OQP), E demonstrates the altered version of OC, with the last note replaced by white noise (OW), F shows the rising intonation version of OW, with a 15% pitch increase in the sixth component (OWP). It is worth noting that the rising intonation in the last components (OCP and OQP) results in measurable alterations in the frequency spectrum profiles of the last components compared to their corresponding original versions (OCP vs. OC and OQP vs. OQ). However, only minor alterations of the last components were observed for OWP and OW.