Auditory neural networks involved in attention modulation prefer biologically significant sounds and exhibit sexual dimorphism in anurans.

Allocating attention to biologically relevant stimuli in a complex environment is critically important for survival and reproductive success. In humans, attention modulation is regulated by the frontal cortex, and is often reflected by changes in specific components of the event-related potential (ERP). Although brain networks for attention modulation have been widely studied in primates and avian species, little is known about attention modulation in amphibians. The present study aimed to investigate the attention modulation networks in an anuran species, the Emei music frog (Babina daunchina). Male music frogs produce advertisement calls from within underground nest burrows that modify the acoustic features of the calls, and both males and females prefer calls produced from inside burrows. We broadcast call stimuli to male and female music frogs while simultaneously recording electroencephalographic (EEG) signals from the telencephalon and mesencephalon. Granger causal connectivity analysis was used to elucidate functional brain networks within the time window of ERP components. The results show that calls produced from inside nests which are highly sexually attractive result in the strongest brain connections; both ascending and descending connections involving the left telencephalon were stronger in males while those in females were stronger with the right telencephalon. Our findings indicate that the frog brain allocates neural attention resources to highly attractive sounds within the window of early components of ERP, and that such processing is sexually dimorphic, presumably reflecting the different reproductive strategies of males and females.

Effect of the Level of Anesthesia on the Auditory Brainstem Response in the Emei Music Frog (Babina daunchina).

Anesthesia is known to affect the auditory brainstem response (ABR) in mice, rats, birds and lizards. The present study investigated how the level of anesthesia affects ABR recordings in an amphibian species, Babina daunchina. To do this, we compared ABRs evoked by tone pip stimuli recorded from 35 frogs when Tricaine methane sulphonate (MS-222) anesthetic immersion times varied from 0, 5 and 10 minutes after anesthesia induction at sound frequencies between 0.5 and 6 kHz. ABR thresholds increased significantly with immersion time across the 0.5 kHz to 2.5 kHz frequency range, which is the most sensitive frequency range for hearing and the main frequency range of male calls. There were no significant differences for anesthetic levels across the 3 kHz to 6 kHz range. ABR latency was significantly longer in the 10 min group than in the 0 and 5 min groups at frequencies of 0.5, 1.0, 1.5, 2.5 kHz, while ABR latency did not differ across the 3 kHz to 4 kHz range and at 2.0 kHz. Taken together, these results show that the level of anesthesia affects the amplitude, threshold and latency of ABRs in frogs.

Sound Classification and Call Discrimination Are Decoded in Order as Revealed by Event-Related Potential Components in Frogs.

Species that use communication sounds to coordinate social and reproductive behavior must be able to distinguish vocalizations from nonvocal sounds as well as to identify individual vocalization types. In this study we sought to identify the neural localization of the processes involved and the temporal order in which they occur in an anuran species, the music frog Babina daunchina. To do this we measured telencephalic and mesencephalic event-related potentials (ERPs) elicited by synthesized white noise (WN), highly sexually attractive (HSA) calls produced by males from inside nests and male calls of low sexual attractiveness (LSA) produced outside of nests. Each stimulus possessed similar temporal structures. The results showed the following: (1) the amplitudes of the first negative ERP component (N1) at ∼ 100 ms differed significantly between WN and conspecific calls but not between HSA and LSA calls, indicating that discrimination between conspecific calls and nonvocal sounds occurs in ∼ 100 ms, (2) the amplitudes of the second positive ERP component (P2) at ∼ 200 ms in the difference waves between HSA calls and WN were significantly higher than between LSA calls and WN in the right telencephalon, implying that call characteristic identification occurs in ∼ 200 ms and (3) WN evoked a larger third positive ERP component (P3) at ∼ 300 ms than conspecific calls, suggesting the frogs had classified the conspecific calls into one category and perceived WN as novel. Thus, both the detection of sounds and the identification of call characteristics are accomplished quickly in a specific temporal order, as reflected by ERP components. In addition, the most dynamic ERP patterns appeared in the left mesencephalon and the right telencephalon, indicating the two brain regions might play key roles in anuran vocal communication.

The biological significance of acoustic stimuli determines ear preference in the music frog.

Behavioral and neurophysiological studies support the idea that right ear advantage (REA) exists for perception of conspecific vocal signals in birds and mammals. Nevertheless, few studies have focused on anuran species that typically communicate through vocalization. The present study examined the direction and latencies of orientation behaviors in Emei music frogs (Babina daunchina) produced in response to six auditory stimuli emitted by a speaker placed directly behind the subjects. The stimuli included male advertisement calls produced from within burrow nests, which have been shown to be highly sexually attractive (HSA), calls produced from outside burrows, which are of low sexual attractiveness (LSA), screech calls produced when frogs are attacked by snakes, white noise, thunder and silence. For all sound stimuli except the screech, the frogs preferentially turned to the right. Right ear preference was strongest for HSA calls. For the screech and thunder stimuli, there was an increased tendency for subjects to move further from the speaker rather than turning. These results support the idea that in anurans, right ear preference is associated with perception of positive or neutral signals such as the conspecific advertisement call and white noise, while a left ear preference is associated with perception of negative signals such as predatory attack.

Right ear advantage for vocal communication in frogs results from both structural asymmetry and attention modulation.

Right-ear/left-hemisphere advantage (REA) in processing species-specific vocalizations has been demonstrated in mammals including humans. Two models for REA are typically proposed, a structural model and an attentional model. These hypotheses were tested in an anuran species, the Emei music frog (Babina daunchina) in which females strongly prefer male calls produced from inside mud-retuse burrows (high sexual attractiveness or HSA calls) to those produced in open fields (low sexual attractiveness or LSA calls). Isochronic playbacks were used to control for attention to stimuli presented to either the left or right sides of female subjects while electroencephalogram (EEG) signals were recorded from the left and right midbrain and telencephalon. The results show that relative EEG power in the delta band declined while those of the alpha and beta bands increased with time in the left but not the right midbrain. Since the anuran midbrain receives auditory information derived primarily from the contralateral auditory nerve, these results support the idea that REA occurs in frogs because communication sounds are processed preferentially in the left midbrain. Furthermore, though differences in the dynamic changes of the delta, alpha and beta bands in the left midbrain between acoustic stimuli were not statistically significant, these changes were stronger during the playback of HSA calls toward which females tend to allocate greater attentional resources. These results imply that REA in frogs results from the combined effects of structural asymmetry and attention modulation.

Mating signals indicating sexual receptiveness induce unique spatio-temporal EEG theta patterns in an anuran species.

Female mate choice is of importance for individual fitness as well as a determining factor in genetic diversity and speciation. Nevertheless relatively little is known about how females process information acquired from males during mate selection. In the Emei music frog, Babina daunchina, males normally call from hidden burrows and females in the reproductive stage prefer male calls produced from inside burrows compared with ones from outside burrows. The present study evaluated changes in electroencephalogram (EEG) power output in four frequency bands induced by male courtship vocalizations on both sides of the telencephalon and mesencephalon in females. The results show that (1) both the values of left hemispheric theta relative power and global lateralization in the theta band are modulated by the sexual attractiveness of the acoustic stimulus in the reproductive stage, suggesting the theta oscillation is closely correlated with processing information associated with mate choice; (2) mean relative power in the beta band is significantly greater in the mesencephalon than the left telencephalon, regardless of reproductive status or the biological significance of signals, indicating it is associated with processing acoustic features and (3) relative power in the delta and alpha bands are not affected by reproductive status or acoustic stimuli. The results imply that EEG power in the theta and beta bands reflect different information processing mechanisms related to vocal recognition and auditory perception in anurans.

Contact-call driven and tone-driven zenk expression in the nucleus ovoidalis of the budgerigar (Melopsittacus undulatus).

The effectiveness of species-typical contact calls and a 3-kHz pure tone to induce zenk gene protein expression in the primary thalamic auditory relay nucleus ovoidalis was compared in budgerigars (Melopsittacus undulatus), a parrot species capable of lifelong vocal learning. Ovoidalis consists of a core which projects topographically to field L of the telencephalon and a ventromedial shell containing many calcitonin-gene-related peptide neurons that project throughout field L as well as to an adjacent field receiving visual input. Tone-induced and call-induced zenk expression in the ovoidalis core were similar; however, call-induced zenk expression in ventromedial ovoidalis shell was significantly greater than tone-induced expression. These results support the idea that the ovoidalis shell may contain neurons specialized to process complex sounds including species-typical communication sounds.

Feeding and contact call stimulation both induce zenk and cfos expression in a higher order telencephalic area necessary for vocal learning in budgerigars.

Stimulation with natural contact calls and feeding were used to assess zenk and fos protein expression in budgerigars (Melopsittacus undulatus), a vocal learning parrot species in which feeding and physical contact often occur in conjunction with vocalization. Although only calls induced gene expression in Field L, the primary telencephalic auditory area, both calls and feeding induced gene expression in the frontal lateral nidopallium (NFl), a brain area in receipt of input from Field L which projects to areas afferent to vocal control nuclei and which is necessary for new call learning. NFl thus appears poised to provide both non-auditory as well as auditory feedback to the vocal system.

Contact call-driven zenk mRNA expression in the brain of the budgerigar (Melopsittacus undulatus).

Contact call-driven zenk (zif268, egr1, NGF1A, Krox 24) mRNA expression was mapped with in situ hybridization histochemistry in a vocal learning parrot, the budgerigar (M. undulatus). Relative to controls, call stimulation induced high zenk mRNA expression in all auditory areas including those closely associated with the vocal system within the anterior forebrain (Brauth et al. (2001) J. Comp. Neurol. 432, 481; (2002) Learn. Memory 9, 76). Thus there is a high correspondence between the distributions of neurons exhibiting contact call-driven zenk protein and mRNA expression in budgerigars. Field L2a, an area reported previously to express only perinucleolar zenk protein localization (Brauth et al. (2002) Learn. Memory 9, 76) also showed zenk mRNA expression.