Publications

Abstract

Vocal learning, the ability to produce modified vocalizations via learning from acoustic signals, is a key trait in the evolution of speech. While extensively studied in songbirds, mammalian models for vocal learning are rare. Bats present a promising study system given their gregarious natures, small size, and the ability of some species to be maintained in captive colonies. We utilize the pale spear-nosed bat (Phyllostomus discolor) and report advances in establishing this species as a tractable model for understanding vocal learning. We have taken an interdisciplinary approach, aiming to provide an integrated understanding across genomics (Part I), neurobiology (Part II), and transgenics (Part III). In Part I, we generated new, high-quality genome annotations of coding genes and noncoding microRNAs to facilitate functional and evolutionary studies. In Part II, we traced connections between auditory-related brain regions and reported neuroimaging to explore the structure of the brain and gene expression patterns to highlight brain regions. In Part III, we created the first successful transgenic bats by manipulating the expression of FoxP2, a speech-related gene. These interdisciplinary approaches are facilitating a mechanistic and evolutionary understanding of mammalian vocal learning and can also contribute to other areas of investigation that utilize P. discolor or bats as study species.

Abstract

Comparative studies of vocal learning and vocal non-learning animals can increase our understanding of the neurobiology and evolution of vocal learning and human speech. Mammalian vocal learning is understudied: most research has either focused on vocal learning in songbirds or its absence in non-human primates. Here we focus on a highly promising model species for the neurobiology of vocal learning: grey seals. We provide a neuroanatomical atlas (based on dissected brain slices and magnetic resonance images), a labelled MRI template, a 3D model with volumetric measurements of brain regions, and histological cortical stainings. Four main features of the grey seal brain stand out. (1) It is relatively big and highly convoluted. (2) It hosts a relatively large temporal lobe and cerebellum, structures which could support developed timing abilities and acoustic processing. (3) The cortex is similar to humans in thickness and shows the expected six-layered mammalian structure. (4) Expression of FoxP2 - a gene involved in vocal learning and spoken language - is present in deeper layers of the cortex. Our results could facilitate future studies targeting the neural and genetic underpinnings of mammalian vocal learning, thus bridging the research gap from songbirds to humans and non-human primates.Competing Interest StatementThe authors have declared no competing interest.

Abstract

Vocal production learning (VPL) is the capacity to learn to produce new vocalizations, which is a rare ability in the animal kingdom and thus far has only been identified in a handful of mammalian taxa and three groups of birds. Over the last few decades, approaches to the demonstration of VPL have varied among taxa, sound production systems and functions. These discrepancies strongly impede direct comparisons between studies. In the light of the growing number of experimental studies reporting VPL, the need for comparability is becoming more and more pressing. The comparative evaluation of VPL across studies would be facilitated by unified and generalized reporting standards, which would allow a better positioning of species on any proposed VPL continuum. In this paper, we specifically highlight five factors influencing the comparability of VPL assessments: (i) comparison to an acoustic baseline, (ii) comprehensive reporting of acoustic parameters, (iii) extended reporting of training conditions and durations, (iv) investigating VPL function via behavioural, perception-based experiments and (v) validation of findings on a neuronal level. These guidelines emphasize the importance of comparability between studies in order to unify the field of vocal learning.

Abstract

Genes including FOXP2, FOXP1 and CNTNAP2, have been implicated in human speech and language phenotypes, pointing to a role in the development of normal language-related circuitry in the brain. Although speech and language are unique human phenotypes, a comparative approach is possible by addressing language-relevant traits in animal model systems. One such trait, vocal learning, represents an essential component of human spoken language, and is shared by cetaceans, pinnipeds, elephants, some birds and bats. Given their vocal learning abilities, gregarious nature, and reliance on vocalisations for social communication and navigation, bats represent an intriguing mammalian system in which to explore language-relevant genes. We used immunohistochemistry to detail the distribution of FoxP2, FoxP1 and Cntnap2 proteins, accompanied by detailed cytoarchitectural histology in the brains of two vocal learning bat species; Phyllostomus discolor and Rousettus aegyptiacus. We show widespread expression of these genes, similar to what has been previously observed in other species, including humans. A striking difference was observed in the adult Phyllostomus discolor bat, which showed low levels of FoxP2 expression in the cortex, contrasting with patterns found in rodents and non-human primates. We created an online, open-access database within which all data can be browsed, searched, and high resolution images viewed to single cell resolution. The data presented herein reveal regions of interest in the bat brain and provide new opportunities to address the role of these language-related genes in complex vocal-motor and vocal learning behaviours in a mammalian model system.