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Review
. 2010 Dec;20(6):754-63.
doi: 10.1016/j.conb.2010.08.021. Epub 2010 Sep 20.

The behavioral neuroscience of anuran social signal processing

Affiliations
Review

The behavioral neuroscience of anuran social signal processing

Walter Wilczynski et al. Curr Opin Neurobiol. 2010 Dec.

Abstract

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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Figures

Figure 1
Figure 1
Aspects of social signal processing in the nervous system of anuran amphibians, superimposed on schematic dorsal view of a frog brain showing the basic ascending auditory pathways (not all connections are shown). Rostral is at the top, caudal at the bottom. List of abbreviations: Components of the VIIIth cranial nerve complex: G VIII vestibulocochlear nerve ganglion; N VIII vestibulocochlear nerve; AP amphibian papilla; BP basilar papilla; AVC anterior vertical canal; PVC posterior vertical canal; HC horizontal canal; S sacculus; L lagena. Lower brainstem auditory areas: CN caudal nucleus; DLN dorsal lateral nucleus; SON superior olivary nucleus; NLL nucleus of the lateral lemniscus. Midbrain torus semicircularis subdivisions: Tl laminar nucleus; Tm magnocellular nucleus; Tp principal nucleus. Diencephalon: A anterior thalamic nucleus; C central thalamic nucleus; P posterior thalamic nucleus; VM ventromedial thalamic nucleus; SC suprachiasmatic nucleus. Telencephalon: Pm medial pallium; Sep septal complex; Str striato-pallidal complex. Illustration of frog brain and connections from[11]. A. Processes involved in the analysis of conspecific social signals as information ascends from the ear though the brain. 1. Neural responses in the ear generated by two auditory end organs, the amphibian and basilar papillae, are biased toward the spectral features of the conspecific call. 2. As information ascends from the lower brainstem to the midbrain, responses properties of cells become more specialized for coding elemental spectral and temporal features of the conspecific call. 3. In the midbrain, many neurons act as specialized feature detectors for either spectral or temporal call characteristics, which in turn relay this information to forebrain areas regulating motor and physiological responses to the call. However, the call is best represented there by activity distributed in multiple midbrain neurons across its subnuclei, that is, by a process of population coding. 4. In addition to changes in the firing rates of neurons within brain nuclei, behavioral salient signals like conspecific social signals induce changes in the correlated patterns of activity locally and across brain divisions, that is, a change in the functional connectivity of brain areas. B. Coding of acoustic social signals at different levels of the frog nervous system. In the brainstem (medulla and midbrain), neural activity is driven by sensory features of the signal. Activity in thalamic nuclei is correlated with sensory features and movement during the stimulus period. Telencephalic activity in most areas is more strongly correlated with movement than with stimulus features. The torus semicricularis of the midbrain (circled in red) is a key gateway for transferring sensory information from lower levels to the motor and endocrine control areas of the forebrain and its properties are important for generating sex differences in responding as well as changes in responding with physiological state.
Figure 2
Figure 2
Matrix indicating patterns of correlated activity, measured by level of egr-1 expression, across regions of the telencephalon, hypothalamus, thalamus, and midbrain (coded by gray scale) when Physalaemus pustulosus frogs heard a heterospecific Physalaemus enesefae advertisement call (upper left), a conspecific aggressive call (the mew, upper right), a conspecific advertisement calls (the whine, lower left), or silence. Positive correlations are in yellow, negative in blue, and no significant correlation is indicated by black. When hearing a conspecific advertisement call, neural activation within and across brain regions becomes significantly more correlated indicating a change in functional connectivity. From[38].
Figure 3
Figure 3
Relative expression of egr-1 in the superior olivary nucleus (A) and laminar nucleus of the torus semicircularis (B) in male (gray bars) and female (black bars) túngara frogs hearing a conspecific Physalaemus pustulosus advertisement call, a heterospecific Physalaemus petersi advertisement call, or silence. The results show that the superior olivary nucleus, a lower brainstem auditory center, responds best to the conspecific call in both sexes and there is no sex difference. In the midbrain, however, male neural response is equally strong to the conspecific and heterospecific calls, whereas female responses are significantly lower to the heterospecific call. This matches the behavioral response: males will call in response to either call, whereas females express phonotaxis only to the conspecific call. Modified from[49].
Figure 4
Figure 4
Three possible mechanisms of could account for differences in the responses to male social signals between sexes, among individuals with in a sex, or within an individual depending on physiological state or external conditions. A. Sensory systems may be different, thereby biasing responses at higher levels. B. A neural locus acting as a ‘gateway’ controls access to behavioral control centers so that information transfer to higher behavioral or physiological response areas is different. C. Both the sensory processing and the transfer of information is constant, but the behavioral control centers have different thresholds, filter functions, or other characteristics leading to the behavioral differences. Immediate early gene results in túngara frogs suggest that the most likely possible mechanism is B, with the gateway being the midbrain auditory center relaying information about calls to forebrain areas controlling motor and endocrine functions. Figure courtesy of K. Hoke.

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References

    1. Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W, editors. The Evoution of the Amphibian Auditory System. New York: Wiley; 1988.
    1. Narins PN, Feng AS, Fay RR, Popper AN, editors. Hearing and Sound Communication in Amphibians. New York: Springer-Verlag; 2007.
    1. Ryan MJ, editor. Anuran Communication. Washington DC: Smithsonian Institution Press; 2001.
    1. Wells KD. The social behavior of anuran amphibians. Animal Behaviour. 1977;25:666–693. Well’s paper is an excellent, comprehensive review of the literature on anuran acoustic communication up to its publication date. It is widely considered a starting point for background information and general overview of anuran acoustic communication across species, including male signaling and both male and female responses.
    1. Ryan MJ, Bernal XE, Rand AS. Female mate choice and the potential for ornament evolution in túngara frogs. Physalaemus pustulosus Current Zoology. 2010;56:343–357. Ryan et al. review experimental studies of female mate choice in túngara frogs to examine an important general issue in evolutionary animal behavior, the evolution elaborate male signals. The authors show that a variety of additions to the conspecific mate recognition signal, both naturally occurring and artificial, enhance the attractiveness of the call to females. The authors argue that latent female preferences for a variety of signal elaborations or innovations can drive the evolution of male signals.

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