Abstract
The ability to vocalize is ubiquitous in vertebrates, but neural networks underlying vocal control remain poorly understood. Here, we performed simultaneous neuronal recordings in the frontal cortex and dorsal striatum (caudate nucleus, CN) during the production of echolocation pulses and communication calls in bats. This approach allowed us to assess the general aspects underlying vocal production in mammals and the unique evolutionary adaptations of bat echolocation. Our data indicate that before vocalization, a distinctive change in high-gamma and beta oscillations (50-80 Hz and 12-30 Hz, respectively) takes place in the bat frontal cortex and dorsal striatum. Such precise fine-tuning of neural oscillations could allow animals to selectively activate motor programs required for the production of either echolocation or communication vocalizations. Moreover, the functional coupling between frontal and striatal areas, occurring in the theta oscillatory band (4-8 Hz), differs markedly at the millisecond level, depending on whether the animals are in a navigational mode (that is, emitting echolocation pulses) or in a social communication mode (emitting communication calls). Overall, this study indicates that fronto-striatal oscillations could provide a neural correlate for vocal control in bats.
Highlights
Vocalization-based interactions between broadcaster and receiver play an important role in everyday life scenarios and are highly conserved throughout the animal kingdom [1,2]
To assess fronto-striatal network activity during vocalization, 47 extracellular, paired recordings were acquired from the frontal auditory field (FAF) and the caudate nucleus (CN) of the dorsal striatum of four male bats
Striatal recordings were performed with linear tetrodes, while FAF activity was measured with linear 16-channel probes
Summary
Vocalization-based interactions between broadcaster and receiver play an important role in everyday life scenarios and are highly conserved throughout the animal kingdom [1,2]. Rhythmic neural activity ( known as oscillations) in striatal structures such as the caudate, putamen, and nucleus accumbens has been linked to speech production in healthy humans, to disorders such as stuttering [3], and to diseases that involve speech impairments such as Parkinson disease and Tourette syndrome [4,5,6] To date, it remains largely discussed how (and if) oscillations in neural networks involving the striatum participate in the precise control of vocal motor outputs in humans and other vertebrate species. Vocal production correlates well with distinct inter-areal coupling in the theta band and specialized intraareal processing mechanisms in the gamma and beta bands of LFPs. Taken together, our results present correlative evidence for the involvement of fronto-striatal circuits in motor action-pattern selection to produce different vocal outputs
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