Brain evolution by brain pathway duplication

Abstract

Understanding the mechanisms of evolution of brain pathways for complex behaviours is still in its infancy. Making further advances requires a deeper understanding of brain homologies, novelties and analogies. It also requires an understanding of how adaptive genetic modifications lead to restructuring of the brain. Recent advances in genomic and molecular biology techniques applied to brain research have provided exciting insights into how complex behaviours are shaped by selection of novel brain pathways and functions of the nervous system. Here, we review and further develop some insights to a new hypothesis on one mechanism that may contribute to nervous system evolution, in particular by brain pathway duplication. Like gene duplication, we propose that whole brain pathways can duplicate and the duplicated pathway diverge to take on new functions. We suggest that one mechanism of brain pathway duplication could be through gene duplication, although other mechanisms are possible. We focus on brain pathways for vocal learning and spoken language in song-learning birds and humans as example systems. This view presents a new framework for future research in our understanding of brain evolution and novel behavioural traits.

Keywords: brain evolution; brain pathway; duplication; parrots; song systems; speech.

Figure 1.

Brain pathways controlling song in songbirds and spoken language in humans. (a) Vocal learning song pathway of songbirds. (b) Spoken language pathway of humans. Black arrows, posterior vocal motor pathway; white arrows, anterior vocal learning pathway; dashed arrows, connections between the two pathways; red arrows, specialized direct projection from forebrain to brainstem vocal MN in vocal learners. Italicized letters indicate that these regions mainly show motor (m), auditory (a), equally both motor and auditory (m/a) neural activity or activity-dependent gene expression in awake animals. Adapted from [2,50]. Not all connections are shown, for simplicity. Some connections in the human brain are proposed based on known connectivity of adjacent brain regions in non-human primates. A1–L4, primary auditory cortex—layer 4; Am, nucleus ambiguous; aSt, anterior striatum; Av, avalanche; aDLM, anterior dorsolateral nucleus of the thalamus; DM, dorsal medial nucleus of the midbrain; HVC, a vocal nucleus (no abbreviation); L2, field L2; LMC, laryngeal motor cortex; LSC, laryngeal somatosensory cortex; NIf, interfacial nucleus of the nidopallium; MAN, magnocellular nucleus of the anterior nidopallium; MN, motor neurons; MO, oval nucleus of the anterior mesopallium; PAG, peri-aqueductal gray; RA, robust nucleus of the arcopallium; v, ventricle space.

Figure 2.

Hypothesis of evolution of song system in parrots owing to sequential pathway duplications. (a) The parrot ancestral motor pathway (light green) with the posterior motor connections (in black arrows) and the anterior motor connections (in white arrows). (b) The parrot core song system (red), proposed to have evolved out of the pre-existing motor pathway through duplication. (c) The parrot shell song system (yellow), proposed to have evolved out of a partial duplication of the core song system. Black arrows, posterior vocal motor pathway; white arrows, anterior vocal motor pathway; dashed arrows, connections between the two pathways; red arrow, specialized direct projection from forebrain to brainstem vocal MN in vocal learners. Connectivity based on summaries in [39,55,56,76,83,84]. See fig. 20 from Chakraborty et al. [56] for additional connections of the core and shell song pathways. Not all connections are shown for simplicity, including reciprocal connections and additional thalamic projections. AAC, central nucleus of the anterior arcopallium; Ai, intermediate arcopallium; AM, anterior mesopallium; AN, anterior nidopallium; ASt, anterior striatum; B, basorostralis; DM, dorsal medial nucleus of the midbrain; DMM, magnocellular nucleus of the dorsomedial thalamus; DT, dorsal thalamus; L2, L4, auditory areas; NAO, oval nucleus of the anterior nidopallium; NCL, nidopallium caudal lateral; NLC, central nucleus of the lateral nidopallium; PMN, premotor neurons; LAN, lateral nucleus of the anterior nidopallium; LAM, lateral nucleus of the anterior mesopallium; MMSt, magnocellular nucleus of the medial striatum; MO, oval nucleus of the anterior mesopallium; PLM, posterior lateral mesopallium; PLN, posterior lateral nidopallium; XII, 12th motor nucleus.