Sexually dimorphic sensory gating drives behavioral differences in túngara frogs

Hoke, Kim L.; Ryan, Michael J.; Wilczynski, Walter

doi:10.1242/jeb.043992

Cited by 33 publications

(31 citation statements)

References 27 publications

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“…In receptive female túngara frogs ( Engystomops pustulosus ), exposure to conspecific male calls induced Egr-1 expression in the ventral striatum (Chakraborty et al, 2010; cf. Hoke et al, 2010), suggesting that reward pathways may respond to courtship vocalizations in frogs as well as songbirds. Thus, although our findings may show that music and song induce similar responses in the listeners, these responses may be shared also by other animals listening to sounds that are much less musical.…”

Section: Resultsmentioning

confidence: 99%

Birdsong: Is It Music to Their Ears?

Earp¹,

Maney²

2012

Front. Evol. Neurosci.

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Since the time of Darwin, biologists have wondered whether birdsong and music may serve similar purposes or have the same evolutionary precursors. Most attempts to compare song with music have focused on the qualities of the sounds themselves, such as melody and rhythm. Song is a signal, however, and as such its meaning is tied inextricably to the response of the receiver. Imaging studies in humans have revealed that hearing music induces neural responses in the mesolimbic reward pathway. In this study, we tested whether the homologous pathway responds in songbirds exposed to conspecific song. We played male song to laboratory-housed white-throated sparrows, and immunolabeled the immediate early gene product Egr-1 in each region of the reward pathway that has a clear or putative homologue in humans. We found that the responses, and how well they mirrored those of humans listening to music, depended on sex and endocrine state. In females with breeding-typical plasma levels of estradiol, all of the regions of the mesolimbic reward pathway that respond to music in humans responded to song. In males, we saw responses in the amygdala but not the nucleus accumbens – similar to the pattern reported in humans listening to unpleasant music. The shared responses in the evolutionarily ancient mesolimbic reward system suggest that birdsong and music engage the same neuroaffective mechanisms in the intended listeners.

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Section: Resultsmentioning

confidence: 99%

Birdsong: Is It Music to Their Ears?

Earp¹,

Maney²

2012

Front. Evol. Neurosci.

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“…These results suggest that the midbrain is a key component of the neural mechanisms generating sex differences in responding to social signals, and it acts by regulating the range of signals passing from the auditory system to the forebrain. Examining the functional connectivity between midbrain and forebrain also implicates the torus as a gateway contributing to the sex differences in behavioral responses to signals[47]. In females, there is a significant linear correlation between laminar nucleus IEG expression and forebrain expression; in males, the correlation is not significant.…”

Section: Sex Differences In Responding To Signalsmentioning

confidence: 99%

“…Somewhat surprisingly, the patterns of correlation among forebrain nuclei do not differ in males and females despite sex differences in IEG expression in several forebrain areas[47]. This suggests that once activated, forebrain areas work together similarly in males and females, again indicating that the midbrain link between auditory processing in the brainstem, and forebrain operations underlying behavioral responses, is the key to generating sex differences in behavior.…”

Section: Sex Differences In Responding To Signalsmentioning

confidence: 99%

The behavioral neuroscience of anuran social signal processing

Wilczynski

Ryan

2010

Current Opinion in Neurobiology

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Acoustic communication is the major component of social behavior in anuran amphibians (frogs and toads) and has served as a neuroethological model for the nervous system's processing of social signals related to mate choice decisions. The male's advertisement or mating call is its most conspicuous social signal, and the nervous system's analysis of the call is a progressive process. As processing proceeds through neural systems, response properties become more specific to the signal and, in addition, neural activity gradually shifts from representing sensory (auditory periphery and brainstem) to sensorimotor (diencephalon) to motor (forebrain) components of a behavioral response.A comparative analysis of many anuran species shows that the first stage in biasing responses toward conspecific signals over heterospecific signals, and toward particular features of conspecific signals, lies in the tuning of the peripheral auditory system. Biases in processing signals are apparent through the brainstem auditory system, where additional feature detection neurons are added by the time processing reaches the level of the midbrain. Recent work using immediate early gene expression as a marker of neural activity suggests that by the level of the midbrain and forebrain, the differential neural representation of conspecific and heterospecific signals involves both changes in mean activity levels across multiple subnuclei, and in the functional correlations among acoustically active areas. Our data show that in frogs the auditory midbrain appears to play an important role in controlling behavioral responses to acoustic social signals by acting as a regulatory gateway between the stimulus analysis of the brainstem and the behavioral and physiological control centers of the forebrain. We predict that this will hold true for other vertebrate groups such as birds and fish that produce acoustic social signals, and perhaps also in fish where electroreception or vibratory sensing through the lateral line systems plays a role in social signaling, as in all these cases ascending sensory information converges onto midbrain nuclei which relay information to higher brain centers.

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“…The torus is a midbrain auditory processing area that is equivalent to the inferior colliculus of mammals and has previously been shown to respond selectively to stimulation with conspecific calls in other frog species (Burmeister et al, 2008;Hoke et al, 2004;Hoke et al, 2008;Leary et al, 2008). The torus is also a critical part of the auditory system for connecting sensory processing with both motor and endocrine areas of the forebrain (Hoke et al, 2008;Hoke et al, 2010;Wilczynski and Ryan, 2010). We hypothesized that ecologically relevant exposure to mate signals would increase expression of the activity-dependent immediate early gene egr-1 in the torus in response to mate attraction signals.…”

Section: Introductionmentioning

confidence: 99%

Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations

Gall

Wilczynski

2014

Journal of Experimental Biology

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There is a long history in neuroethology of investigating how communication signals influence the brain and behavior. It has become increasingly clear that brain areas associated with sensory processing are plastic in adults and that this plasticity is related to reproductive condition. However, the role of communication signal reception in adult auditory plasticity has received relatively little attention. Here, we investigated whether the reception of communication signals (a frog chorus) could enhance the responsiveness of the auditory system to future reception of communication signals (a single male call). We found that animals that had been exposed to 10 days of a male chorus had stronger auditory midbrain immediate early gene expression than animals that had been exposed to 10 days of random tones when tested with 30 min of male calls or 30 min of tones. Our results suggest that exposure to dynamic social stimuli, like frog choruses, may play an important role in shaping the neural and behavioral responses to communication signals.

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Sexually dimorphic sensory gating drives behavioral differences in túngara frogs

Cited by 33 publications

References 27 publications

Birdsong: Is It Music to Their Ears?

Birdsong: Is It Music to Their Ears?

The behavioral neuroscience of anuran social signal processing

Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations

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