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 forebrain may 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.     

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.     

Testosterone alters genomic responses to song and monoaminergic innervation of auditory areas in a seasonally breeding songbird

Behavioral responses to social stimuli often vary according to endocrine state. Our previous work has suggested that such changes in behavior may be due in part to hormone‐dependent sensory processing. In the auditory forebrain of female white‐throated sparrows, expression of the immediate early gene ZENK (egr‐1) is higher in response to conspecific song than to a control sound only when plasma estradiol reaches breeding‐typical levels. Estradiol also increases the number of detectable noradrenergic neurons in the locus coeruleus and the density of noradrenergic and serotonergic fibers innervating auditory areas. We hypothesize, therefore, that reproductive hormones alter auditory responses by acting on monoaminergic systems. This possibility has not been examined in males. Here, we treated non‐breeding male white‐throated sparrows with testosterone to mimic breeding‐typical levels and then exposed them to conspecific male song or frequency‐matched tones. We observed selective ZENK responses in the caudomedial nidopallium only in the testosterone‐treated males. Responses in another auditory area, the caudomedial mesopallium, were selective regardless of hormone treatment. Testosterone treatment reduced serotonergic fiber density in the auditory forebrain, thalamus, and midbrain, and although it increased the number of noradrenergic neurons detected in the locus coeruleus, it reduced noradrenergic fiber density in the auditory midbrain. Thus, whereas we previously reported that estradiol enhances monoaminergic innervation of the auditory pathway in females, we show here that testosterone decreases it in males. Mechanisms underlying testosterone‐dependent selectivity of the ZENK response may differ from estradiol‐dependent ones.© 2013 Wiley Periodicals, Inc. Develop Neurobiol 73: 455–468, 2013     

Candidate neural locus for sex differences in reproductive decisions

Sexual selection and signal detection theories predict that females should be selective in their responses to mating signals in mate choice, while the response of males to signals in male competition should be less selective. The neural processes underlying this behavioural sex difference remain obscure. Differences in behavioural selectivity could result from differences in how sensitive sensory systems are to mating signals, distinct thresholds in motor areas regulating behaviour, or sex differences in selectivity at a gateway relaying sensory information to motor systems. We tested these hypotheses in frogs using the expression of egr-1 to quantify the neural responses of each sex to mating signals. We found that egr-1 expression in a midbrain auditory region was elevated in males in response to both conspecific and heterospecific calls, whereas in females, egr-1 induction occurred only in response to conspecific signals. This differential neural selectivity mirrored the sex differences in behavioural responsiveness to these stimuli. By contrast, egr-1 expression in lower brainstem auditory centres was not different in males and females. Our results support a model in which sex differences in behavioural selectivity arise from sex differences in the neural selectivity in midbrain areas relaying sensory information to the forebrain.     

An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog

The matched filter hypothesis proposes that the tuning of auditory sensitivity and the spectral character of calls will match in order to maximize auditory processing efficiency during courtship. In this study, we analyzed the acoustic structure of male calls and both male and female hearing sensitivities in the little torrent frog (Amolops torrentis), an anuran species who transmits acoustic signals across streams. The results were in striking contradiction to the matched filter hypothesis. Auditory brainstem response results showed that the best hearing range was 1.6–2 kHz consistent with the best sensitive frequency of most terrestrial lentic taxa, yet completely mismatched with the dominant frequency of conspecific calls (4.3 kHz). Moreover, phonotaxis tests show that females strongly prefer high‐frequency (4.3 kHz) over low‐frequency calls (1.6 kHz) regardless of ambient noise levels, although peripheral auditory sensitivity is highest in the 1.6–2 kHz range. These results are consistent with the idea that A. torrentis evolved from nonstreamside species and that high‐frequency calls evolved under the pressure of stream noise. Our results also suggest that female preferences based on central auditory system characteristics may evolve independently of peripheral auditory system sensitivity in order to maximize communication effectiveness in noisy environments.     

Neurophysiological response selectivity for conspecific songs over synthetic sounds in the auditory forebrain of non-singing female songbirds

Female choice plays a critical role in the evolution of male acoustic displays. Yet there is limited information on the neurophysiological basis of female songbirds’ auditory recognition systems. To understand the neural mechanisms of how non-singing female songbirds perceive behaviorally relevant vocalizations, we recorded responses of single neurons to acoustic stimuli in two auditory forebrain regions, the caudal lateral mesopallium (CLM) and Field L, in anesthetized adult female zebra finches (Taeniopygia guttata). Using various metrics of response selectivity, we found consistently higher response strengths for unfamiliar conspecific songs compared to tone pips and white noise in Field L but not in CLM. We also found that neurons in the left auditory forebrain had lower response strengths to synthetics sounds, leading to overall higher neural selectivity for song in neurons of the left hemisphere. This laterality effect is consistent with previously published behavioral data in zebra finches. Overall, our results from Field L are in parallel and from CLM are in contrast with the patterns of response selectivity reported for conspecific songs over synthetic sounds in male zebra finches, suggesting some degree of sexual dimorphism of auditory perception mechanisms in songbirds.     

仙琴蛙对不同类型声音的感知差异研究

既往研究发现听觉感知包括对声音信号的觉察、感觉、注意和知觉等多个认知过程,但依然不清楚大脑如何对不同类型的复杂声音信号(如同种鸣声和其他声音)进行解码和处理,以及在感知不同类型声音信号时大脑活动的动态特征.本研究记录了在随机播放白噪声和洞内鸣叫声音刺激时仙琴蛙Nidirana daunchina的左右端脑、间脑和中脑的...     

Flexibility as a Strategy for Avoiding Call Overlap in Male Anhui Treefrogs

Male-male vocal competition is critical for mating success in anuran species; however, it remains unknown that how males regulate their competitive strategies dynamically during competition because calling is highly time-consuming, energetically demanding and likely to increase predation risks. Since different parts of calls will encode different information for vocal communication, we hypothesized that competitive strategies of male frogs may be modulated by the temporal and spectral features of different call notes. To test this hypothesis, the natural advertisement calls(OC), its modified versions with the first call note replaced by white noise(WN) or other notes and with the fifth call note replaced by WN, were played back to the Anhui tree frogs(Rhacophorus zhoukaiyae). Results showed that 1) males produced more competitive calls in response to acoustic stimuli compared to their baseline calling during silence; and 2) males emitted more non-overlapping calls compared to overlapping calls in response to the acoustic stimuli. These results are consistent with the idea that males are flexible to acoustic signals and their competition strategies are modulated dynamically by social contexts.     

Female sexual arousal in amphibians

Rather than being a static, species specific trait, reproductive behavior in female amphibians is variable within an individual during the breeding season when females are capable of reproductive activity. Changes in receptivity coincide with changes in circulating estrogen. Estrogen is highest at the point when females are ready to choose a male and lay eggs. At this time female receptivity (her probability of responding to a male vocal signal) is highest and her selectivity among conspecific calls (measured by her probability of responding to a degraded or otherwise usually unattractive male signal) is lowest. These changes occur even though females retain the ability to discriminate different acoustic characteristics of various conspecific calls. After releasing her eggs, female amphibians quickly become less receptive and more choosy in terms of their responses to male sexual advertisement signals. Male vocal signals stimulate both behavior and estrogen changes in amphibian females making mating more probable. The changes in female reproductive behavior are the same as those generally accepted as indicative of a change in female sexual arousal leading to copulation. They are situationally triggered, gated by interactions with males, and decline with the consummation of sexual reproduction with a chosen male. The changes can be triggered by either internal physiological state or by the presence of stimuli presented by males, and the same stimuli change both behavior and physiological (endocrine) state in such a way as to make acceptance of a male more likely. Thus amphibian females demonstrate many of the same general characteristics of changing female sexual state that in mammals indicate sexual arousal.     

Hearing conspecific vocal signals alters peripheral auditory sensitivity

We investigated whether hearing advertisement calls over several nights, as happens in natural frog choruses, modified the responses of the peripheral auditory system in the green treefrog, Hyla cinerea. Using auditory evoked potentials (AEP), we found that exposure to 10 nights of a simulated male chorus lowered auditory thresholds in males and females, while exposure to random tones had no effect in males, but did result in lower thresholds in females. The threshold change was larger at the lower frequencies stimulating the amphibian papilla than at higher frequencies stimulating the basilar papilla. Suprathreshold responses to tonal stimuli were assessed for two peaks in the AEP recordings. For the peak P1 (assessed for 0.8–1.25 kHz), peak amplitude increased following chorus exposure. For peak P2 (assessed for 2–4 kHz), peak amplitude decreased at frequencies between 2.5 and 4.0 kHz, but remained unaltered at 2.0 kHz. Our results show for the first time, to our knowledge, that hearing dynamic social stimuli, like frog choruses, can alter the responses of the auditory periphery in a way that could enhance the detection of and response to conspecific acoustic communication signals.     

Multiple signals and male spacing affect female preference at cocktail parties in treefrogs

Effective acoustic communication in the face of intense conspecific background noise constitutes a constant sensory challenge in chorusing and colonial species. An evolutionary approach suggests that behavioural and environmental constraints in these species should have shaped signal design and signalling behaviour to enable communication in noisy conditions. This could be attained both through the use of multicomponent signals and through short-term adjustments in the spatial separation of calling males. We investigated these two hypotheses in a chorusing anuran, the hylid Hyla arborea, through a series of phonotaxis experiments conducted within a six-speaker arena in a high background noise situation, by presenting females with male calls containing either single or multiple attractive call components, and by modifying distances between speakers. We found that female ability to discriminate attractive calls increased when several attractive call components were available, providing novel evidence that the use of multicomponent signals enhances communication in complex acoustic conditions. Signal discrimination in females also improved with speaker separation, demonstrating that within natural choruses, spatial unmasking conditioned by male density and spatial separation probably improves female discrimination of competing males. Implications of these results for the accuracy of mate choice within choruses are discussed.     

Spatially-mediated call pattern recognition and the cocktail party problem in treefrog choruses: can call frequency differences help during signal overlap?

Male gray treefrogs, Hyla versicolor, advertise for mates in dense assemblages characterized by high levels of noise and acoustic clutter. In pairwise interactions, males alternate pulsatile advertisement calls and so reduce call overlap to levels below that expected by chance. However, in choruses consisting of more than two males, acoustic interference increases dramatically. Moreover, males do not seem to exhibit selective attention in a way that reduces call interference among nearest neighbours. Previous research has also demonstrated that although females discriminate strongly against overlapped calls, negative effects of call overlap can be attenuated by a large angular separation between signal sources. However, call stimuli employed were identical in spectrum and so this situation differs from that likely in nature. Based on studies of ‘auditory stream segregation’ with other taxa, we hypothesized that realistic differences in the frequencies of overlapping calls could improve the ability of females to discern critical call features during overlap of separated call sources. We found that, although, under some circumstances, differences in call frequency may help females distinguish among neighbouring males giving temporally proximate calls, naturalistic spectral differences do not seem to help females perceptually separate the overlapping calls of neighbouring conspecific males.     

Integration of sensory and motor processing underlying social behaviour in túngara frogs

Social decision making involves the perception and processing of social stimuli, the subsequent evaluation of that information in the context of the individual's internal and external milieus to produce a decision, and then culminates in behavioural output informed by that decision. We examined brain networks in an anuran communication system that relies on acoustic signals to guide simple, stereotyped motor output. We used egr-1 mRNA expression to measure neural activation in male túngara frogs, Physalaemus pustulosus, following exposure to conspecific and heterospecific calls that evoke competitive or aggressive behaviour. We found that acoustically driven activation in auditory brainstem nuclei is transformed into activation related to sensory-motor interactions in the diencephalon, followed by motor-related activation in the telencephalon. Furthermore, under baseline conditions, brain nuclei typically have correlated egr-1 mRNA levels within brain divisions. Hearing conspecific advertisement calls increases correlations between anatomically distant brain divisions; no such effect was observed in response to calls that elicit aggressive behaviour. Neural correlates of social decision making thus take multiple forms: (i) a progressive shift from sensory to motor encoding from lower to higher stages of neural processing and (ii) the emergence of correlated activation patterns among sensory and motor regions in response to behaviourally relevant social cues.     

The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

Juvenile male zebra finches develop their song by imitation. Females do not sing but are attracted to males' songs. With functional magnetic resonance imaging and event‐related potentials we tested how early auditory experience shapes responses in the auditory forebrain of the adult bird. Adult male birds kept in isolation over the sensitive period for song learning showed no consistency in auditory responses to conspecific songs, calls, and syllables. Thirty seconds of song playback each day over development, which is sufficient to induce song imitation, was also sufficient to shape stimulus‐specific responses. Strikingly, adult females kept in isolation over development showed responses similar to those of males that were exposed to songs. We suggest that early auditory experience with songs may be required to tune perception toward conspecific songs in males, whereas in females song selectivity develops even without prior exposure to song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2010     

Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway

Catecholaminergic (CA) neurons innervate sensory areas and affect the processing of sensory signals. For example, in birds, CA fibers innervate the auditory pathway at each level, including the midbrain, thalamus, and forebrain. We have shown previously that in female European starlings, CA activity in the auditory forebrain can be enhanced by exposure to attractive male song for one week. It is not known, however, whether hearing song can initiate that activity more rapidly. Here, we exposed estrogen-primed, female white-throated sparrows to conspecific male song and looked for evidence of rapid synthesis of catecholamines in auditory areas. In one hemisphere of the brain, we used immunohistochemistry to detect the phosphorylation of tyrosine hydroxylase (TH), a rate-limiting enzyme in the CA synthetic pathway. We found that immunoreactivity for TH phosphorylated at serine 40 increased dramatically in the auditory forebrain, but not the auditory thalamus and midbrain, after 15 min of song exposure. In the other hemisphere, we used high pressure liquid chromatography to measure catecholamines and their metabolites. We found that two dopamine metabolites, dihydroxyphenylacetic acid and homovanillic acid, increased in the auditory forebrain but not the auditory midbrain after 30 min of exposure to conspecific song. Our results are consistent with the hypothesis that exposure to a behaviorally relevant auditory stimulus rapidly induces CA activity, which may play a role in auditory responses.     

Female reproductive state influences the auditory midbrain response

Female behavioral responses to sensory stimuli can be highly variable across the reproductive cycle. Female green treefrogs (Hyla cinerea) use the male vocal signal to locate and choose a mate. Gravid females approach a vocalizing male to mate but do not approach if they have recently mated. Such differences in behavioral response may be due in part to shifts in the neural representation of auditory information in the brain. In this study, we investigated the influence of female reproductive state on neural responses in the auditory midbrain to both communication signals (advertisement calls) and non-communication sounds (band limited noise bursts). Recently mated females exhibited significantly reduced response strengths compared to females not recently mated. Reduced response strengths in post-mated females were in response to both noise bursts and male advertisement calls but were limited to the lower frequency range corresponding to the amphibian papilla of the peripheral auditory system. Our results therefore show that the ability of social signals to stimulate the auditory system differs in females depending on their reproductive state, and that the differential effect on low versus high spectral sensitivities may influence the way the two spectral peaks of male advertisement calls are represented.     

Female frog auditory sensitivity,male calls,and background noise: potential influences on the evolution of a peculiar matched filter

The matched filter hypothesis proposes that the tuning of females' auditory sensitivity matches the spectral energy distribution of males' signals. Such correspondence is expected to arise over evolutionary time, as it promotes conspecific information transfer and reduces interference from other sound sources. Our main objective was to determine the correspondence between the acoustic sensitivity of female frogs of Eupsophus roseus and the spectral characteristics of advertisement vocalizations produced by conspecific males. We also aimed to determine how auditory sensitivity is related to the characteristics of background noise. We analysed data on the auditory sensitivity of E. roseus females, and recordings of conspecific male vocalizations and of the acoustic environment during the breeding period of this species. Our results indicate a concordance between the auditory sensitivity of females and call spectra that would provide an appropriate detection of these signals. In addition, this matching is large relative to the correspondence between auditory sensitivity with the spectra of the abiotic and biotic background noise, with the last component being associated with calls of the related species Eupsophus vertebralis. This may be an adaptation of receivers confronting sound interference, which improves the capability of E. roseus to communicate sexually by means of acoustic signals. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 814–827.     

Ultrasound hearing and male–male communication in Australian katydids (Tettigoniidae: Zaprochilinae) with sexually dimorphic ears

The genus Kawanaphila (Tettigoniidae: Zaprochilinae) is unusual among the Tettigoniidae in the possession of sexually dimorphic auditory organs. We examined the auditory system and acoustic behaviour of two previously unstudied species in this genus to test whether reduced hearing in males is consistently associated with reduced male–male competition. Kawanaphila yarraga (Rentz, 1993) and K. mirla (Rentz, 1993) are both sexually dimorphic with respect to their auditory system, but to different degrees. Males of both species produce songs consisting of trains of brief (< 1 ms) pure-tone sound pulses at ultrasonic frequencies (K. yarraga, 40 kHz;K. mirla, 70 kHz). In both species, female hearing is more sensitive than that of males by 10 dB. In addition, male K. mirla are most sensitive at lower frequencies than females. Male and female K. yarraga differed only in sensitivity, not in tuning. The two species also differ in their degree of sexual dimorphism in auditory anatomy. Kawanaphila mirla males lack some auditory specializations of the prothoracic tracheal system, which are present in the normal tettigoniid condition in females. In K. yarraga males these structures are present, but reduced in size relative to females. The acoustic behaviour of males of the two species is consistent with this pattern of relative auditory sensitivity. Males of both species interact acoustically by altering the timing of their sound output to synchronize with neighbouring males. However, K. mirla males only interact in this way over very short distances (< 5 m), whereas K. yarraga males interact with neighbours up to at least 10 m distant. These results indicate that, although males of the two species differ in hearing sensitivity, the nature of their responses to conspecific calls are similar to one another and to those of other acoustic insects. This suggests that acoustically mediated male–male competition may be maintained even while selection favours a reduction in male auditory sensitivity.     

Female mate choice and the potential for ornament evolution in túngara frogs Physalaemus pustulosus

The potential for ornament evolution in response to sexual selection rests on the interaction between the permissive-ness or selectivity of female preferences and the constraints on male development of signaling related traits. We investigate the former by determining how latent female preferences either exaggerate the magnitude of current traits (I.e. Elaborations) or favor novel traits (I.e. Innovations). In tungara frogs, females prefer complex mating calls (whine-chucks) to simple calls (whine only). The whine is critical for mate recognition while the chuck further enhances the attractiveness of the call. Here we use a combina-tion of synthetic and natural stimuli to examine latent female preferences. Our results show that a diversity of stimuli, including conspecific and heterospecific calls as well as predator-produced and human-made sounds, increase the attractiveness of a call when added to a whine. These stimuli do not make simple calls more attractive than a whine-chuck, however. In rare cases we found stimuli that added to the whine decrease the attractiveness of the call. Overall, females show strong preferences for both elaborations and innovations of the chuck. We argue that the emancipation of these acoustic adornments from mate recognition allows such female permissiveness, and that male constraints on signal evolution are probably more important in explaining why males evolved their specific adornment. Experimentally probing latent female preferences for stimuli out of the species' range is a useful means to gain insights about the potential of female choice to influence signal evolution and thus the astounding diversity in male sexually-selected traits.     

Neural Activity Patterns in Response to Interspecific and Intraspecific Variation in Mating Calls in the Túngara Frog

Background

During mate choice, individuals must classify potential mates according to species identity and relative attractiveness. In many species, females do so by evaluating variation in the signals produced by males. Male túngara frogs (Physalaemus pustulosus) can produce single note calls (whines) and multi-note calls (whine-chucks). While the whine alone is sufficient for species recognition, females greatly prefer the whine-chuck when given a choice.

Methodology/Principal Findings

To better understand how the brain responds to variation in male mating signals, we mapped neural activity patterns evoked by interspecific and intraspecific variation in mating calls in túngara frogs by measuring expression of egr-1. We predicted that egr-1 responses to conspecific calls would identify brain regions that are potentially important for species recognition and that at least some of those brain regions would vary in their egr-1 responses to mating calls that vary in attractiveness. We measured egr-1 in the auditory brainstem and its forebrain targets and found that conspecific whine-chucks elicited greater egr-1 expression than heterospecific whines in all but three regions. We found no evidence that preferred whine-chuck calls elicited greater egr-1 expression than conspecific whines in any of eleven brain regions examined, in contrast to predictions that mating preferences in túngara frogs emerge from greater responses in the auditory system.

Conclusions

Although selectivity for species-specific signals is apparent throughout the túngara frog brain, further studies are necessary to elucidate how neural activity patterns vary with the attractiveness of conspecific mating calls.