Brain evolution by brain pathway duplication

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“One of the duplicated genes may then acquire a mutation in coding or regulatory sequences, which enables it to acquire a new function that then undergoes selection, a process known as neofunctionalization [12–15].”

“With the recent availability of genomes across the avian [93,177,178] and eventually primate [179,180] family trees, it becomes possible to discover candidate genes.”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“One overall hypothesis is that significant changes in the brain can be generated by novel gene functions owing to gene duplications or expansion of gene regulatory networks [7,9–12].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“The brain also has evolved in a mosaic pattern, with some regions changing dramatically, while others have remained little changed through the course of evolution [23].”

“Duplication itself may modify the selection pressure on both structures, thereby allowing the individual structures to use the once single functional space in a mechanism reminiscent of adaptive radiation [38].”

“Many animals, such as annelids, have repeated parallel body segments or specialized limb types among species, where the replicated parts are thought to be owing to a repeating developmental genomic programme [121,122].”

“The pallium is largely layered in mammals, and mostly nuclear in birds, reptiles and other vertebrates, but with divergences among them [24,25].”

“One overall hypothesis is that significant changes in the brain can be generated by novel gene functions owing to gene duplications or expansion of gene regulatory networks [7,9–12].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“During development, neural stem cell/progenitor cells that give rise to forebrain circuits derive mainly from stem cells in the ventricular zone [129–131].”

“During development, neural stem cell/progenitor cells that give rise to forebrain circuits derive mainly from stem cells in the ventricular zone [129–131].”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“The concept of neofunctionalization of genes [14] and subfunctionalization of genes [148] match those proposed for structural duplications [128,149,150].”

“Vocal learning is a rare trait, so far discovered in five distantly related groups of mammals (humans, bats, elephants, cetaceans (dolphins and whales) and pinnipeds (seals and sea lions)) and three distantly related groups of birds (parrots, songbirds and hummingbirds) [1,40–42].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“In this regard, various hypotheses have been proposed to explain evolution of complex behavioural traits, including increases in brain or brain region size relative to body size, increases in total number of neurons or neuron density, and presence versus absence of particular neural networks that control a specific ty…”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“However, such an anatomical position is not present in hummingbirds, parrots, or humans [1,2].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“Allman and Kaas also proposed that development of the brain could be altered owing to a gene mutation so that a given area is duplicated [33,37].”

“SRGAP2 modulates activity of the ROBO axon guidance receptors, which are in turn activated by the SLIT family of protein ligands to modulate axonal/dendritic migration and branching in various brain regions [163–167].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“With the recent availability of genomes across the avian [93,177,178] and eventually primate [179,180] family trees, it becomes possible to discover candidate genes.”

“SRGAP2 modulates activity of the ROBO axon guidance receptors, which are in turn activated by the SLIT family of protein ligands to modulate axonal/dendritic migration and branching in various brain regions [163–167].”

“An example relevant to the topic of vocal learning and cognition is the Slit-Robo GTPase 2 gene (SRGAP2), which has undergone two partial duplications (SRGAP2B and SRGAP2C) uniquely in humans relative to other mammals [26,27,162].”

“Vocal learning is a rare trait, so far discovered in five distantly related groups of mammals (humans, bats, elephants, cetaceans (dolphins and whales) and pinnipeds (seals and sea lions)) and three distantly related groups of birds (parrots, songbirds and hummingbirds) [1,40–42].”

“Many invertebrates and Amphioxus possess one Hox gene cluster, whereas the remaining vertebrates have four Hox gene clusters, in part owing to two whole-genome duplication events that occurred early in vertebrate evolution [151,154–158].”

“An example of loss of gene function and functional redundancy leading to duplication of structure is the Mauthner (M) cells, a pair of reticulospinal neurons that control escape behaviour in zebra fishes [139,172–174].”

“An example relevant to the topic of vocal learning and cognition is the Slit-Robo GTPase 2 gene (SRGAP2), which has undergone two partial duplications (SRGAP2B and SRGAP2C) uniquely in humans relative to other mammals [26,27,162].”

“[101,102] showed that there is a comparable area 44-like region involved in orofacial musculature functions in macaque monkeys.”

“Adapted from [2,50].”

“An example of loss of gene function and functional redundancy leading to duplication of structure is the Mauthner (M) cells, a pair of reticulospinal neurons that control escape behaviour in zebra fishes [139,172–174].”

“Once daughter cells reach their target location in the brain, they find their connecting partners in a process that requires cell adhesion and axon guidance genes [137,138].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“[101,102] showed that there is a comparable area 44-like region involved in orofacial musculature functions in macaque monkeys.”

“Both the core and shell song regions were functionally active in the production of learned vocalizations, as revealed by vocalizing-driven immediate early gene expression (EGR-1, C-FOS and DUSP-1), whereas the surrounding brain regions were active in production of non-singing motor behaviour, as revealed by rhythmic c…”

“These are transcription factors that control the anterior–posterior body plan axis and are situated in the genome in the same order as the body plan they control [136,151,152].”

“A long proposed explanation for generating increased cortical complexity is that a single region gradually differentiates into two or more areas [30–35].”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“differential gene expression experiments, which show that the avian pallium has a functional columnar organization similar to the mammalian pallial domain [39,52–54].”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“differential gene expression experiments, which show that the avian pallium has a functional columnar organization similar to the mammalian pallial domain [39,52–54].”

“SRGAP2 modulates activity of the ROBO axon guidance receptors, which are in turn activated by the SLIT family of protein ligands to modulate axonal/dendritic migration and branching in various brain regions [163–167].”

“Connectivity based on summaries in [39,55,56,76,83,84].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“It would be exciting to determine if similar duplications of brain pathways have occurred in humans, not only in the speech pathways but also for other advanced motor movements such as dancing [97–99].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“One overall hypothesis is that significant changes in the brain can be generated by novel gene functions owing to gene duplications or expansion of gene regulatory networks [7,9–12].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“They do so by controlling regional neuronal identity, stem cell progenitors, cell migration and cell death [159,160].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“With the recent availability of genomes across the avian [93,177,178] and eventually primate [179,180] family trees, it becomes possible to discover candidate genes.”

“Some such changes may have occurred with the emergence of the telencephalon during the invertebrate to vertebrate transition, indicating that the central nervous system has been an important target of selection [4,6–8].”

“Many invertebrates and Amphioxus possess one Hox gene cluster, whereas the remaining vertebrates have four Hox gene clusters, in part owing to two whole-genome duplication events that occurred early in vertebrate evolution [151,154–158].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“Both the core and shell song regions were functionally active in the production of learned vocalizations, as revealed by vocalizing-driven immediate early gene expression (EGR-1, C-FOS and DUSP-1), whereas the surrounding brain regions were active in production of non-singing motor behaviour, as revealed by rhythmic c…”

“Overall, structural duplications have been proposed to be one mechanism that allows for morphological decoupling [126].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“The daughter cells travel to their positions either by radial migration perpendicularly away from the ventricle (such as excitatory neurons within layers of the mammalian cortex), and/or by tangential migration parallel to the ventricle (such as inhibitory neurons that migrate from the basal ganglia into the cortex) […”

“The concept of neofunctionalization of genes [14] and subfunctionalization of genes [148] match those proposed for structural duplications [128,149,150].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“differential gene expression experiments, which show that the avian pallium has a functional columnar organization similar to the mammalian pallial domain [39,52–54].”

“Their local brain region identity is thought to be controlled by patterning transcription factors, such as the homeobox (Hox) genes [135,136].”

“Both the core and shell song regions were functionally active in the production of learned vocalizations, as revealed by vocalizing-driven immediate early gene expression (EGR-1, C-FOS and DUSP-1), whereas the surrounding brain regions were active in production of non-singing motor behaviour, as revealed by rhythmic c…”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“Even theories on gene evolution through gene duplication have influenced the theories on brain evolution by morphological duplication [139,141].”

“Since all of the cortex is connected with all of the basal ganglia and thalamus [112], when a cortex region is duplicated, one would expect to see a concomitant duplication in the connected basal ganglia and thalamic regions [22,33].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“Connectivity based on summaries in [39,55,56,76,83,84].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Since all of the cortex is connected with all of the basal ganglia and thalamus [112], when a cortex region is duplicated, one would expect to see a concomitant duplication in the connected basal ganglia and thalamic regions [22,33].”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“Many invertebrates and Amphioxus possess one Hox gene cluster, whereas the remaining vertebrates have four Hox gene clusters, in part owing to two whole-genome duplication events that occurred early in vertebrate evolution [151,154–158].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“A striking example of independently evolved morphological duplications is the diversification of the adductor mandibular muscles in teleost fish jaws, which have independently subdivided several times during tetraodontiform evolution [123–125].”

“The daughter cells travel to their positions either by radial migration perpendicularly away from the ventricle (such as excitatory neurons within layers of the mammalian cortex), and/or by tangential migration parallel to the ventricle (such as inhibitory neurons that migrate from the basal ganglia into the cortex) […”

“auditory Field L), but in parrots it receives additional auditory input from a small part of the nucleus basorostralis (B), the remainder of which is somatosensory [81].”

“Recently, based on comparative genomic analyses across the bird family tree, unique gene duplications were found in the songbird lineage and some of these genes had enriched or nearly exclusive expression in the song learning nuclei [161].”

“Some such changes may have occurred with the emergence of the telencephalon during the invertebrate to vertebrate transition, indicating that the central nervous system has been an important target of selection [4,6–8].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“In addition, changes in the regulation of some genes that may allow greater vocal–motor–auditory integration in vocal learning systems could have influenced changes in the surrounding motor areas to allow greater auditory–motor entrainment and synchronizing of body movements to the rhythm of music for dance in parrots…”

“Even theories on gene evolution through gene duplication have influenced the theories on brain evolution by morphological duplication [139,141].”

“The daughter cells travel to their positions either by radial migration perpendicularly away from the ventricle (such as excitatory neurons within layers of the mammalian cortex), and/or by tangential migration parallel to the ventricle (such as inhibitory neurons that migrate from the basal ganglia into the cortex) […”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“In this regard, various hypotheses have been proposed to explain evolution of complex behavioural traits, including increases in brain or brain region size relative to body size, increases in total number of neurons or neuron density, and presence versus absence of particular neural networks that control a specific ty…”

“They do so by controlling regional neuronal identity, stem cell progenitors, cell migration and cell death [159,160].”

“An example relevant to the topic of vocal learning and cognition is the Slit-Robo GTPase 2 gene (SRGAP2), which has undergone two partial duplications (SRGAP2B and SRGAP2C) uniquely in humans relative to other mammals [26,27,162].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Second, analyses of brain gene expression profiles strongly suggest that songbirds and parrots independently evolved vocal learning pathways by duplication of preexisting, surrounding motor circuits (57, 58).”

“Chakraborty & Jarvis (2015) further observed that parrots, which are the most accomplished avian vocal learners, possess nested “shell” and “core” vocal systems.”

“It thus may not take many generations of captive breeding before a parrot such as the budgerigar no longer acts, vocalizes, or develops in the ways that it did in nature.”

“Additional support for a duplication theory also comes from genetic profiling analyses comparing gene expressions in song-learning birds and humans (Pfenning et al. 2014; Chakraborty and Jarvis 2015).”

“First, the specialized neural mechanisms that underpin vocal learning (Bolhuis et al., 2010; Chakraborty et al., 2015; Feenders et al., 2008; Jarvis, 2004) may be difficult to evolve (Chakraborty & Jarvis, 2015; Isler & Schaik, 2006; Mink et al., 1981).”

“Moreover, Psittacines and Passeriformes are both vocal learners, and thus their cerebral bauplan includes unique vocal and auditory nuclei, which are not present in nonvocal learners (Chakraborty & Jarvis, 2015; Reiner, Perkel, Mello, & Jarvis, 2004).”

“The expanded toolkit of nervous genes likely provided opportunities for regulatory network rewiring and new functions to evolve (Chakraborty and Jarvis 2015; Evlampiev and Isambert 2007; Oakley and Rivera 2008).”

“It has been proposed that analogous modifications have occurred in the human lineage [39].”

“Under this model, increased behavioural precision, or diversi fi cation, can occur through replication of established cell types and circuits within generally conserved networks 4,5 .”

“Consistent with these observations, a strong case has been made that vocal learning brain pathways evolved out of motor-learning pathways that control complex, learned nonvocal behaviors (Feenders et al. 2008, Tokarev et al. 2011, Chakraborty & Jarvis 2015, Jarvis 2019).”

“Indeed, Chakraborty and Jarvis [54] acknowledge it might not be straightforward to reconcile the core/shell system with the VLC. Finally, in the VLC, humans alone are considered high-end vocal learners, whereas parrots are classified at a level just below, referred to as complex vocal learners.”

“songbirds and humans share the rare and remarkable suite of traits for learned vocalizations (Chakraborty and Jarvis, 2015; Prather et al., 2017), understanding the role of neuroestrogens in communication learning and processing may lead to important translational dis-”

“…expansion of forebrain size and increased pallium (i.e., cortical) neuron density in song-birds ’ and parrots ’ brains (Olkowicz et al. 2016), which in turn may have accommodated their extra vocal learning brain pathway (Feenders et al. 2008; Chakraborty and Jarvis 2015; Chakraborty et al. 2015).”

“However, the evolution of brain pathways that promote complex behavioral traits remains enigmatic [43].”

“Similar mechanisms have been proposed to underlie the elaboration of cerebellar nuclei 59 and the evolution of pallial–striatal circuits 58 in vertebrates.”

“In mammals, it has been proposed that brain pathways can arise via duplication and subspecialization, and thus elaborate over evolutionary time analogously to gene duplication (Chakraborty and Jarvis, 2015).”

“4, blue lines), respectively, which is called ‘song system’ (Konishi 1985; Brainard & Doupe 2000; Matsunaga & Okanoya 2009; Mooney 2009; Chakraborty & Jarvis 2015).”

“Vocal learning circuits in birds are thought to have evolved via the duplication and modification of ancestral motor circuits (29).”

“Duplication and divergence of circuits was also proposed as a possible mechanism for the evolution of brain pathways for vocal learning in song-learning birds, spoken language in humans ( Chakraborty and Jarvis, 2015 ) and other circuits ( Roberts et al., 2022 ).”

“Genetic duplication and adoption from the pre-existing spinal GRPR neural circuits could be possible mechanisms by which neural circuits of contagious itch arose during evolution (Chakraborty and Jarvis, 2015).”

“2 Schematic of core and shell systems for vocal learning in a parrot brain [83].”

“Chakraborty & Jarvis (2015) proposed that such a phenotype could arise by mutations that cause the entire network to duplicate as an ensemble, in line with a previous proposal that the avian song system itself may have evolved as a specialization from a pre-existing limb and body motor network…”

“…by the laryngeal motor cortex (LMC), connect directly to vocal motor neurons (plain red arrows, lower panel) providing the motor output (controlling the larynx in humans or syrinx in birds) [14], [15]. is also called vocal production pathway, since it involves direct projections to motor neurons.”

“Even more puzzling, from a functional point of view, is, as Chakraborty and colleagues [38,39] discovered, that parrots have a core and shell song systems, i.”

“The neuronal circuitry that generates these signals includes forebrain and midbrain regions and a single or multiple hindbrain vocal central pattern generators (CPGs, e.g., Bass, 2014; Chakraborty & Jarvis, 2015).”

“For example, circuits involved in avian song production [57,58] and electroreception in mormyrid fishes [17] likely involved circuit replication, while a specific conserved circuit motif is duplicated during cerebellar expansion in vertebrates [59].”

“At the neural level, though the songbird and parrot song systems are both nucleated and contain distinct anterior and posterior pathways, there are also important differences in the detailed connectivity likely related to the distinct effects of AFP inactivations 18–27 .”

“One possibility, is that the specialized neural mechanisms that underpin vocal learning (Bolhuis and Wynne 2009; Chakraborty and Jarvis 2015; Jarvis 2004) may simple be difficult to evolve on a structural or technical level (Chakraborty and Jarvis 2015; Isler and van Schaik 2006; Mink et al. 1981).”

“In a revised scenario, HVC neurons might have evolved from ancestral motor circuits through duplication (Chakraborty & Jarvis, 2015) or the strengthening of these pathways (Petkov & Jarvis, 2012) that later specialized for vocal con-trol (Feenders et al., 2008).”

“For these reasons, it is proposed that vocal learning pathways might have arisen by the duplication of brain pathways from surrounding motor learning circuits, which subsequently become specialized for sets of genes involved in neural connectivity, physiology, and plasticity [2,4,7].”

“And why do parrots have an additional shell song control system, i.e. have brain structures meant for song even more complex than in songbirds (Chakraborty and Jarvis, 2015)?”

“striatal circuits of songbirds mediating vocal learning have been proposed to evolve via the duplication and diversification of ancestral motor learning circuits (83, 84).”

“This approach has already led to consolidated theories about the evolution of selected brain modules (Feenders et al., 2008; Chakraborty & Jarvis, 2015; Kebschull et al., 2020) and to increasingly detailed descriptions of the evolutionary origin of the existing modular organization (Cisek, 2019;…”

“Beyond such changes in brain architecture, other influential models predict that modified long-range connectivity among existing brain regions can lead to functional di-vergences [9, 24–26].”

“…output nucleus, sits at the medial end of AId and has similar gene expression and connectivity as its neighbor, suggesting that RA is a specialized motor control region derived from ancestral motor circuitry [Feenders et al., 2008; Chakraborty and Jarvis, 2015; Jarvis, 2019; Nevue et al., 2020].”

“For notice that copying-and-repurposing is quite common in biological evolution (Barrett, 2012; Chakraborty & Jarvis, 2015; Kaas, 1989; Marcus, 2004).”

“…don’t exhibit BPS, is that parrots and humans have a more complex vocal learning system, and (ii) that this complexity is related to the added ability of parrots and humans to control supra-syringeal/laryngeal vocal organs, which seems to involve a dual neural control system in both species [2, 3].”

“…anatomical position and connectivity, several related hypotheses on the evolutionary origin of the song system have suggested that HVC might be a specialized part of NCL that could have diverged from NCL via pathway duplication (Farries 2001; Feenders et al. 2008; Chakraborty and Jarvis 2015).”

“Structure duplication followed by divergence is a driving force in brain evolution 29,30 and is thought to have underlaid the emergence of basal ganglia and cerebellar circuits 31,32 , bird and human vocal pathways 30,33 and higher-order cortical areas from primary sensory and motor ones 34–36 .”

“It have been suggested that the brain nuclei of songbirds have analogous regions in human brain with respect to their role in vocal control (Fig 4A) [36,37].”

“Genetic and developmental mechanisms have been put forward for the duplication of mammalian brain circuits and their divergence to new functions (e.g., Rakic, 2009; Chakraborty and Jarvis, 2015).”

“Such expansion of specific neuronal projections have been proposed to expand behavioural repertoire, such as increased dexterity 23,48 and courtship songs 4 .”