Preference of spectral features in auditory processing for advertisement calls in the music frogs.

BACKGROUND: Animal vocal signals encode very important information for communication during which the importance of temporal and spectral characteristics of vocalizations is always asymmetrical and species-specific. However, it is still unknown how auditory system represents this asymmetrical and species-specific patterns. In this study, auditory event related potential (ERP) changes were evaluated in the Emei music frog (Babina daunchina) to assess the differences in eliciting neural responses of both temporal and spectral features for the telencephalon, diencephalon and mesencephalon respectively. To do this, an acoustic playback experiment using an oddball paradigm design was conducted, in which an original advertisement call (OC), its spectral feature preserved version (SC) and temporal feature preserved version (TC) were used as deviant stimuli with synthesized white noise as standard stimulus. RESULTS: The present results show that 1) compared with TC, more similar ERP components were evoked by OC and SC; and 2) the P3a amplitudes in the forebrain evoked by OC were significantly higher in males than in females. CONCLUSIONS: Together, the results provide evidence for suggesting neural processing for conspecific vocalization may prefer to the spectral features in the music frog, prompting speculation that the spectral features may play more important roles in auditory object perception or vocal communication in this species. In addition, the neural processing for auditory perception is sexually dimorphic.

Auditory perception exhibits sexual dimorphism and left telencephalic dominance in Xenopus laevis.

Sex differences in both vocalization and auditory processing have been commonly found in vocal animals, although the underlying neural mechanisms associated with sexual dimorphism of auditory processing are not well understood. In this study we investigated whether auditory perception exhibits sexual dimorphism in Xenopus laevis To do this we measured event-related potentials (ERPs) evoked by white noise (WN) and conspecific calls in the telencephalon, diencephalon and mesencephalon respectively. Results showed that (1) the N1 amplitudes evoked in the right telencephalon and right diencephalon of males by WN are significantly different from those evoked in females; (2) in males the N1 amplitudes evoked by conspecific calls are significantly different from those evoked by WN; (3) in females the N1 amplitude for the left mesencephalon was significantly lower than for other brain areas, while the P2 and P3 amplitudes for the right mesencephalon were the smallest; in contrast these amplitudes for the left mesencephalon were the smallest in males. These results suggest auditory perception is sexually dimorphic. Moreover, the amplitude of each ERP component (N1, P2 and P3) for the left telencephalon was the largest in females and/or males, suggesting that left telencephalic dominance exists for auditory perception in Xenopus.

The right thalamus may play an important role in anesthesia-awakening regulation in frogs.

BACKGROUND: Previous studies have shown that the mammalian thalamus is a key structure for anesthesia-induced unconsciousness and anesthesia-awakening regulation. However, both the dynamic characteristics and probable lateralization of thalamic functioning during anesthesia-awakening regulation are not fully understood, and little is known of the evolutionary basis of the role of the thalamus in anesthesia-awakening regulation. METHODS: An amphibian species, the South African clawed frog (Xenopus laevis) was used in the present study. The frogs were immersed in triciane methanesulfonate (MS-222) for general anesthesia. Electroencephalogram (EEG) signals were recorded continuously from both sides of the telencephalon, diencephalon (thalamus) and mesencephalon during the pre-anesthesia stage, administration stage, recovery stage and post-anesthesia stage. EEG data was analyzed including calculation of approximate entropy (ApEn) and permutation entropy (PE). RESULTS: Both ApEn and PE values differed significantly between anesthesia stages, with the highest values occurring during the awakening period and the lowest values during the anesthesia period. There was a significant correlation between the stage durations and ApEn or PE values during anesthesia-awakening cycle primarily for the right diencephalon (right thalamus). ApEn and PE values for females were significantly higher than those for males. DISCUSSION: ApEn and PE measurements are suitable for estimating depth of anesthesia and complexity of amphibian brain activity. The right thalamus appears physiologically positioned to play an important role in anesthesia-awakening regulation in frogs indicating an early evolutionary origin of the role of the thalamus in arousal and consciousness in land vertebrates. Sex differences exist in the neural regulation of general anesthesia in frogs.

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.

The First Call Note Plays a Crucial Role in Frog Vocal Communication.

Vocal Communication plays a crucial role in survival and reproductive success in most amphibian species. Although amphibian communication sounds are often complex consisting of many temporal features, we know little about the biological significance of each temporal component. The present study examined the biological significance of notes of the male advertisement calls of the Emei music frog (Babina daunchina) using the optimized electroencephalogram (EEG) paradigm of mismatch negativity (MMN). Music frog calls generally contain four to six notes separated approximately by 150 millisecond intervals. A standard stimulus (white noise) and five deviant stimuli (five notes from one advertisement call) were played back to each subject while simultaneously recording multi-channel EEG signals. The results showed that the MMN amplitude for the first call note was significantly larger than for that of the others. Moreover, the MMN amplitudes evoked from the left forebrain and midbrain were typically larger than those from the right counterpart. These results are consistent with the ideas that the first call note conveys more information than the others for auditory recognition and that there is left-hemisphere dominance for processing information derived from conspecific calls in frogs.

Correction: The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko, Gekko subpalmatus.

[This corrects the article DOI: 10.1371/journal.pone.0146677.].

A lateralized functional auditory network is involved in anuran sexual selection.

Right ear advantage (REA) exists in many land vertebrates in which the right ear and left hemisphere preferentially process conspecific acoustic stimuli such as those related to sexual selection. Although ecological and neural mechanisms for sexual selection have been widely studied, the brain networks involved are still poorly understood. In this study we used multi-channel electroencephalographic data in combination with Granger causal connectivity analysis to demonstrate, for the first time, that auditory neural network interconnecting the left and right midbrain and forebrain function asymmetrically in the Emei music frog (Babina daunchina), an anuran species which exhibits REA. The results showed the network was lateralized. Ascending connections between the mesencephalon and telencephalon were stronger in the left side while descending ones were stronger in the right, which matched with the REA in this species and implied that inhibition from the forebrainmay induce REA partly. Connections from the telencephalon to ipsilateral mesencephalon in response to white noise were the highest in the non-reproductive stage while those to advertisement calls were the highest in reproductive stage, implying the attention resources and living strategy shift when entered the reproductive season. Finally, these connection changes were sexually dimorphic, revealing sex differences in reproductive roles.

Resting-state brain networks revealed by granger causal connectivity in frogs.

Resting-state networks (RSNs) refer to the spontaneous brain activity generated under resting conditions, which maintain the dynamic connectivity of functional brain networks for automatic perception or higher order cognitive functions. Here, Granger causal connectivity analysis (GCCA) was used to explore brain RSNs in the music frog (Babina daunchina) during different behavioral activity phases. The results reveal that a causal network in the frog brain can be identified during the resting state which reflects both brain lateralization and sexual dimorphism. Specifically (1) ascending causal connections from the left mesencephalon to both sides of the telencephalon are significantly higher than those from the right mesencephalon, while the right telencephalon gives rise to the strongest efferent projections among all brain regions; (2) causal connections from the left mesencephalon in females are significantly higher than those in males and (3) these connections are similar during both the high and low behavioral activity phases in this species although almost all electroencephalograph (EEG) spectral bands showed higher power in the high activity phase for all nodes. The functional features of this network match important characteristics of auditory perception in this species. Thus we propose that this causal network maintains auditory perception during the resting state for unexpected auditory inputs as resting-state networks do in other species. These results are also consistent with the idea that females are more sensitive to auditory stimuli than males during the reproductive season. In addition, these results imply that even when not behaviorally active, the frogs remain vigilant for detecting external stimuli.

The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko, Gekko subpalmatus.

The design of acoustic signals and hearing sensitivity in socially communicating species would normally be expected to closely match in order to minimize signal degradation and attenuation during signal propagation. Nevertheless, other factors such as sensory biases as well as morphological and physiological constraints may affect strict correspondence between signal features and hearing sensitivity. Thus study of the relationships between sender and receiver characteristics in species utilizing acoustic communication can provide information about how acoustic communication systems evolve. The genus Gekko includes species emitting high-amplitude vocalizations for long-range communication (loud callers) as well as species producing only low-amplitude vocalizations when in close contact with conspecifics (quiet callers) which have rarely been investigated. In order to investigate relationships between auditory physiology and the frequency characteristics of acoustic signals in a quiet caller, Gekko subpalmatus we measured the subjects' vocal signal characteristics as well as auditory brainstem responses (ABRs) to assess auditory sensitivity. The results show that G. subpalmatus males emit low amplitude calls when encountering females, ranging in dominant frequency from 2.47 to 4.17 kHz with an average at 3.35 kHz. The auditory range with highest sensitivity closely matches the dominant frequency of the vocalizations. This correspondence is consistent with the notion that quiet and loud calling species are under similar selection pressures for matching auditory sensitivity with spectral characteristics of vocalizations.