International Journal of Comparative Psychology

We review the molecular basis of the auditory system development and evolution. The auditory periphery evolved by building on the capacity of vestibular hair cells to respond to higher frequency mechanical stimulation. Evolution altered accessory structures to transform vestibular to auditory receptors. Auditory neurons are derived from vestibular neurons, possibly through the expression of the zinc finger protein GATA3. The bHLH gene Neurogenin1 is expressed in the area of the developing vestibular nuclei whereas the bHLH gene Atoh1 is expressed in the developing auditory nuclei. Atoh1 null mice show an almost complete loss of cochlear nuclei. Overall, the ear, sensory neurons and brainstem auditory nuclei show molecular conservation embedded in an organ-specific molecular context. This results in the modification of the developmental pathways governed by these conserved molecules. These data are consistent with the emerging insight that morphological evolution is primarily driven by the modification of gene expression regulation.

Cetaceans (whales and dolphins) use acoustic cues to determine the locations and identities of environmental stimuli within their underwater habitats. Dolphins evolved unique auditory systems for spatially differentiating ultrasonic signals, whereas the larger baleen whales appear to have evolved different mechanisms for localizing lower frequency sound sources. Many of the cues that terrestrial mammals use to localize sounds in air are less well suited for localizing sounds underwater. Nevertheless, cetaceans can localize sounds as well as or better than most terrestrial mammals. Position dependent spectral filtering likely plays an important role in sound localization by toothed whales, whereas phase differences between the ears may be important for baleen whales. However, it is exceedingly difficult to determine how filtering and phase differences contribute to spatial hearing by whales and dolphins because, in contrast to terrestrial mammals, the structures through which cetaceans receive sounds are completely internalized (and thus invisible). Computational models of cetacean auditory processing provide one viable approach to generating testable predictions about the mechanisms cetaceans use to localize and identify sound sources.

Anatomical and experimental data suggesting a slow adaptation of cochlear mechanics are summarized and discussed. All groups of terrestrial vertebrates, possessing advanced hearing—mammals, Archosauria (birds and crocodiles) and lizards—developed intrinsic cochlear specializations, which may adjust cochlear mechanics and therefore adapt hearing to different acoustic environments, or protect the cochlea from excessive mechanical stimuli. Mammalian outer hair cells, several types of supporting cells, hyaline and homogene in birds and crocodiles, and putative contractile cells of the cochlear lateral wall in mammals and in geckos may provide structural basis for the slow mechanical adaptation. Independent appearance of these specializations in animals that developed different cochlear designs may indicate that the maintenance of “mechanical homeostasis” is a common requirement for the highly organized hearing organ.

Interaural time differences (ITDs) are one of the cues used for binaural sound localisation. In birds, ITDs are computed in nucleus laminaris (NL), where a place code of azimuthal location first emerges. In chickens, NL consists of a monolayer of bitufted cells that receive segregated inputs from ipsi- and contralateral nucleus magnocellularis (NM). In barn owls, the monolayer organisation, the bitufted morphology, and the segregation of inputs have been lost, giving rise to a derived organisation that is accompanied by a reorganisation of the auditory place code. Although chickens and barn owls have been the traditional experimental models in which to study ITD coding, they represent distant evolutionary lineages with very different auditory specialisations. Here we examined the structure of NL in several bird lineages. We have found only two NL morphotypes, one of which appears to have emerged in association with high frequency hearing.

This paper evaluates the development of behaviour from the viewpoint of the intelligent and learning dependent cephalopod mollusks as a contrast to that of mammals. They have a short lifespan, commonly one to two years, and most are semelparous, reproducing only near the end of their lifespan. In the first two months of life, Sepia officinalis cuttlefish show drastic limitation on learning of prey choice and capture, gradually acquiring first short-term and then long-term learning over 60 days. This is paralleled by development of the vertical lobe of the brain which processes visually learned information. In the long nonreproductive adulthood, Octopu s species show major flexibility in prey choice and continued mobility across the sea bottom. This results in large behaviour variability within and between individuals and both exploration and simple play-type behaviour. During the short reproductive period, Sepioteuthis sepioidea squid gather for choice and competition, including flexible strategies in use of their skin display system. At the end of the life cycle, Sepia officinalis cuttlefish have a swift decline in memory capacity and also brain degeneration during their short period of senescence. The emphasis on different behaviour capacities during these four stages is contrasted with those of the mammalian model of behaviour development.

A previous experimental study (Reiss & McCowan, 1993) on dolphin vocal learning documented the process and pattern of vocal imitation in bottlenose dolphins ( Tursiops truncatus ). This previous study demonstrated that dolphins spontaneously imitate novel signals when paired with salient environmental events. The acquisition process of the dolphins’ imitations paralleled both the avian and human vocal development literature. Yet this past study did not directly test whether specific contingencies were necessary for vocal imitation by dolphins. The purpose of this study was to investigate the effects of contextual saliency on vocal imitation and acquisition in bottlenose dolphins. Over a six-month study period, we experimentally exposed two infant male bottlenose dolphins and their mothers to six novel computer-generated whistles that were either unpaired or paired with specific contextual events (preferred toy objects). The results demonstrate that acoustic exposure alone was sufficient for spontaneous vocal imitation to occur but that context affects the timing, extent and quality of vocal imitation by bottlenose dolphins.