Molecular Mapping of Movement-Associated Areas in the Avian Brain: A Motor Theory for Vocal Learning Origin

Abstract

Vocal learning is a critical behavioral substrate for spoken human language. It is a rare trait found in three distantly related groups of birds-songbirds, hummingbirds, and parrots. These avian groups have remarkably similar systems of cerebral vocal nuclei for the control of learned vocalizations that are not found in their more closely related vocal non-learning relatives. These findings led to the hypothesis that brain pathways for vocal learning in different groups evolved independently from a common ancestor but under pre-existing constraints. Here, we suggest one constraint, a pre-existing system for movement control. Using behavioral molecular mapping, we discovered that in songbirds, parrots, and hummingbirds, all cerebral vocal learning nuclei are adjacent to discrete brain areas active during limb and body movements. Similar to the relationships between vocal nuclei activation and singing, activation in the adjacent areas correlated with the amount of movement performed and was independent of auditory and visual input. These same movement-associated brain areas were also present in female songbirds that do not learn vocalizations and have atrophied cerebral vocal nuclei, and in ring doves that are vocal non-learners and do not have cerebral vocal nuclei. A compilation of previous neural tracing experiments in songbirds suggests that the movement-associated areas are connected in a network that is in parallel with the adjacent vocal learning system. This study is the first global mapping that we are aware for movement-associated areas of the avian cerebrum and it indicates that brain systems that control vocal learning in distantly related birds are directly adjacent to brain systems involved in movement control. Based upon these findings, we propose a motor theory for the origin of vocal learning, this being that the brain areas specialized for vocal learning in vocal learners evolved as a specialization of a pre-existing motor pathway that controls movement.

Rudimentary substrates for vocal learning in a suboscine

“…Our results may shed light on the evolution of vocal-learning circuits, which have been proposed to have emerged either from a descending auditory pathway that then added a motor function 39,40 ; or, conversely, that motor pathways became overlaid by auditory control 41 . It has been suggested that in pigeons (Columbiformes), part of the Nd and Ai are thought to be homologous to the auditory 'shelf' and the auditory 'cup' adjacent to the oscine HVC and RA respectively.…”

“…NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3082 ARTICLE song and other motor activity that occurs at the same time as birds sing 41 .…”

“…Such elaborate flight manoeuvreing may require a better coordination or reconfiguration of respiratory control from the forebrain. The forebrain respiratory control may subsequently integrate preexisting motor pathway in the arcopallium for the control of flight, jaw, and vocal movement 11,41 , and/or auditory relays 57 , and lead to evolution of vocal learning (see a similar view proposed by Janik and Slater 58 for vocal learning in mammals). Although this 'respiratory control' hypothesis is highly speculative, the diversity of vocal plasticity, syringeal structure, and neural substrate observed among suboscine species suggest further study of suboscines may help unravel the behavioural, genetic, and anatomical origin of vocal learning.…”

Assessing visual requirements for social context-dependent activation of the songbird song system

“…The anatomical terminology used in this paper follows the new avian brain nomenclature (Reiner et al 2004;Jarvis et al 2005) with modifications ( Feenders et al 2008; see abbreviations list). For visually activated areas adjacent to and near the entopallium (E) of the tectofugal pathway that have been called lateral nidopallium and lateral ventral mesopallium, we called them nidopallium adjacent to the entopallium (Ne) and ventral mesopallium near the entopallium (MVe).…”

Radioactive <em>in situ</em> Hybridization for Detecting Diverse Gene Expression Patterns in Tissue

“…Standard in-situ hybridization methods take longer to seal the slides with parafilm, nail polish, and other means, where slides take up a lot of space; (3) It is highly sensitive for low abundance transcripts due to Dextran sulfate and Denhardt's solution in the hybridization buffer 2,13 ; (4) The imaging approach in darkfield yields high contrast images due to taking pictures under darkfield illumination on a dissecting microscope 4,5 . Additionally, It allows sensitive detection of small changes in gene expression, such as in activity-dependent gene expression to identify specific brain regions activated during perception and production of specific behaviors 19 . The limitations relative to non-radioactive protocols are that the latter are clearer in the cellular resolution and location of the mRNA within the cell, and working with emulsion is very sensitive to manipulation and light.…”