Neural basis of sound pattern recognition in anurans

Voice-sensitivity in the auditory cortex of a range of mammals has been proposed to be determined primarily by tuning to conspecific auditory stimuli, but recent human findings indicate a role for a more general tuning to voicelikeness. Vocal emotional valence, a central characteristic of vocalisations, has been linked to the same basic acoustic parameters across species. Comparative neuroimaging revealed that during voice perception, such acoustic parameters modulate emotional valence-sensitivity in auditory cortical regions in both family dogs and humans. To explore the role of voicelikeness in auditory emotional valence-sensitivity across species, here we constructed artificial emotional sounds in two sound categories: voice-like vs. sine-wave sounds, parametrically modulating two main acoustic parameters, f0 and call length. We hypothesised that if mammalian auditory systems are characterised by a general tuning to voicelikeness, voice-like sounds will be processed preferentially, and acoustic parameters for voice-like sounds will be processed differently than for sine-wave sounds - both in dogs and humans. We found cortical areas in both species that responded stronger to voice-like than to sine-wave stimuli, while there were no regions responding stronger to sine-wave sounds in either species. Additionally, we found that in bilateral primary and emotional valence-sensitive auditory regions of both species, the processing of voice-like and sine-wave sounds are modulated by f0 in opposite ways. These results reveal functional similarities between evolutionarily distant mammals for processing voicelikeness and its effect on processing basic acoustic cues of vocal emotions.

Arginine vasotocin (AVT) and its homolog arginine vasopressin (AVP) modulate social behavior, including social communication. In anuran amphibians, male-male competition and female mate choice rely heavily on acoustic signaling. Behavioral experiments show that AVT influences motivation to call and vocal production. It may also influence how males process and respond to socially relevant auditory stimuli, but few studies have explored this possibility in this taxon. Túngara frogs produce a “whine” that is used for species recognition; in competition with other males they append one or more attractive “chucks” to the whine. Frequency modulation in the whine is an important cue for recognizing conspecifics, and gating of conspecific signals begins in the auditory midbrain. We used dynamic playback experiments to investigate the effects of exogenous AVT on males' responses to stimuli with species-typical and altered frequency modulation. We used avoidance of call overlap as evidence that a male recognizes a stimulus as salient and the production of attractive chucks as evidence of his competitive response to a proximate rival. We used call rate, whine duration, and whine frequency as measures of motivation and motor production. Males responded selectively to a stimulus with species-typical frequency modulation. Following treatment with AVT, they increased call rate and altered whines and chucks in a way that suggests increased air flow during the whine. We did not, however, find evidence that treatment with AVT alters the salience of frequency modulation in recognizing and responding to acoustic signals, at least for the stimuli used in this study.

Amphibians have often been selected as experimental animals in brain research for comparative studies. They are tetrapod anamniotes that represent a key model for understanding the water-to-land transition. In amphibians the basic traits of brain organization in amniotes can be already recognized. In the present chapter we deal with the regional anatomy of the amphibian brain (in the three extant orders) focusing mainly on the chemoarchitecture and genoarchitecture, which serve to define anatomical subdivisions that are otherwise indistinct. The new data are interpreted within the framework of the current neuromeric model that helps comparisons across vertebrates.

Many neurons in the central auditory system of a number of species have been found to be sensitive to the duration of sound stimuli. While previous studies have shown that γ-aminobutyric acid (GABA)-ergic inhibitory input is important for duration sensitivity in the inferior colliculus (IC), it is still unknown whether (GABA)-ergic inhibitory input plays an important role in generating duration sensitivity in the cortex. Using free-field sound stimulation and in vivo extracellular recording, we investigated duration sensitivity in primary auditory cortical (AI) neurons of the Nembutal anesthetized albino mouse (Mus musculus, Km) and examined the effect of the GABA_A receptor antagonist bicuculline on AI neuron duration sensitivity. A total of 63 duration tuning curves were measured in AI neurons. Of these, 44% (28/63) exhibited duration sensitive responses, while 43% (27/63) lacked duration sensitivity. The remaining 13% (8/63) exhibited long-pass properties likely reflecting both duration sensitive and insensitive features. We found that duration sensitive neurons had shorter first spike latency (FSL) and longer firing duration (FD) when stimulated with best duration (p < 0.05), while duration insensitive neurons had invariable FSL and FD at different sound durations (p > 0.05). Furthermore, 60% (6/10) of duration sensitive neurons and 75% (3/4) long-pass neurons lost duration sensitivity following bicuculline application. Taken together, our results show that cortical neurons in the albino mouse are sensitive to sound duration, and that GABAergic inhibition may play an important role in the formation of de novo duration sensitivity in AI. The possible mechanism and behavioral significance of duration sensitivity in AI neurons is discussed.

Amphibians have often been selected as experimental animals in brain research for comparative studies. They are tetrapod anamniotes that represent a key model for understanding the water-to-land transition. In amphibians the basic traits of brain organization in amniotes can be already recognized. In the present chapter we deal with the regional anatomy of the amphibian brain (in the three extant orders) focusing mainly on the chemoarchitecture and genoarchitecture, which serve to define anatomical subdivisions that are otherwise indistinct. The new data are interpreted within the framework of the current neuromeric model that helps comparisons across vertebrates.

This study focused on the response properties underlying selectivity for the rate of frequency modulated (FM) sweeps in the auditory cortex of anesthetized C57bl/6 (C57) mice. Linear downward FM sweeps with rates between 0.08 and 20 kHz/ms were tested. We show that at least two different response properties predict FM rate selectivity: sideband inhibition and duration tuning. Sideband inhibition was determined using the two-tone inhibition paradigm in which excitatory and inhibitory tones were presented with different delays. Sideband inhibition was present in the majority (88%, n = 53) of neurons. The spectrotemporal properties of sideband inhibition predicted rate selectivity and exclusion of the sideband from the sweep reduced/eliminated rate tuning. The second property predictive of sweep rate selectivity was duration tuning for tones. Theoretically, if a neuron is selective for the duration that a sweep spends in the excitatory frequency tuning curve, then rate selectivity will ensue. Duration tuning for excitatory tones was present and predicted rate selectivity in ∼34% of neurons (n = 97). Both sideband inhibition and duration tuning predicted rate selectivity equally well, but sideband inhibition was present in a larger percentage of neurons suggesting that it is the dominant mechanism in the C57 mouse auditory cortex. Similar mechanisms shape sweep rate selectivity in the auditory system of bats and mice and movement-velocity selectivity in the visual system, suggesting similar solutions to analogous problems across sensory systems. This study provides baseline data on basic spectrotemporal processing in the C57 strain for elucidation of changes that occur in presbycusis.