Convergent vocal representations in parrot and human forebrain motor networks.

Abstract

Cortical networks for the production of spoken language in humans are organized by phonetic features^1,2, such as articulatory parameters^3,4 and vocal pitch^5,6. Previous research has failed to find an equivalent forebrain representation in other species^7-11. To investigate whether this functional organization is unique to humans, here we performed population recordings in the vocal production circuitry of the budgerigar (Melopsittacus undulatus), a small parrot that can generate flexible vocal output^12-15, including mimicked speech sounds¹⁶. Using high-density silicon probes¹⁷, we measured the song-related activity of a forebrain region, the central nucleus of the anterior arcopallium (AAC), which directly projects to brainstem phonatory motor neurons^18-20. We found that AAC neurons form a functional vocal motor map that reflects the spectral properties of ongoing vocalizations. We did not observe this organizing principle in the corresponding forebrain circuitry of the zebra finch, a songbird capable of more limited vocal learning²¹. We further demonstrated that the AAC represents the production of distinct vocal features (for example, harmonic structure and broadband energy). Furthermore, we discovered an orderly representation of vocal pitch at the population level, with single neurons systematically selective for different frequency values. Taken together, we have uncovered a functional representation in a vertebrate brain that displays unprecedented commonalities with speech-related motor cortices in humans. This work therefore establishes the parrot as an important animal model for investigating speech motor control and for developing therapeutic solutions for addressing a range of communication disorders^22,23.