Convergent transcriptional specializations in the brains of humans and song-learning birds

Pfenning, Andreas R.; Hara, Erina; Whitney, Osceola; Rivas, Miriam V.; Wang, Rui; Roulhac, Petra L.; Howard, Jason T.; Wirthlin, Morgan; Lovell, Peter V.; Ganapathy, Ganeshkumar; Mouncastle, Jacquelyn; Moseley, M. Arthur; Thompson, J. Will; Soderblom, Erik J.; Iriki, Atsushi; Kato, Masaki; Gilbert, M. Thomas P.; Zhang, Guojie; Bakken, Trygve E.; Bongaarts, Angie; Bernard, Amy; Lein, Ed; Mello, Claudio V.; Hartemink, Alexander J.; Jarvis, Erich D.

doi:10.1126/science.1256846

Cited by 420 publications

(513 citation statements)

References 117 publications

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“…PV-expression in the songbird is confined to specific neuronal populations that are especially involved in song-learning [80][81][82]. This finding suggests that PV fulfills a specific function in these neurons that is potentially related to their morphological plasticity in the context of vocal learning (see also [83]); or, alternatively, to their protection against Ca 2+ -toxicity from the highly active neurons that control some of the fastest muscles in the body [84]. Furthermore, in avian as well as in primate species, PV is differentially up-regulated in the vocal motor neurons of vocal learners (learned songs or spoken language) compared to nonlearners [85].…”

Section: Discussionmentioning

confidence: 95%

Reduction in 50-kHz call-numbers and suppression of tickling-associated positive affective behaviour after lesioning of the lateral hypothalamic parvafox nucleus in rats

Roccaro-Waldmeyer

Babalian

Müller

et al. 2016

Behavioural Brain Research

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h i g h l i g h t s• Wistar rats were tickled before and after excitotoxic lesioning of the lateral hypothalamic parvafox nucleus.• Ultrasonic vocalisations (USVs) that were emitted during the tickling of rats and their tendency to approach and follow the experimenter's hand were analysed.• Lesioning was considered successful if the number of parvalbuminimmunoreactive (PV-ir) cells in the area of the parvafox nucleus was reduced beyond a threshold level.• Rats with bilaterally successful lesions manifested the most profound surgery-associated reduction in the number of 50-kHz USVs and in the tendency to approach and follow the experimenter's hand.• Positive correlations were found between each of the four investigated parameters. g r a p h i c a l a b s t r a c tThe parvafox nucleus is located ventrolaterally in the lateral hypothalamic area (LHA). Its core and shell are composed of neurons expressing the calcium-binding protein parvalbumin (PV) and the transcription factor Foxb1, respectively. Given the known functions of the LHA and that the parvafox nucleus receives afferents from the lateral orbitofrontal cortex and projects to the periaqueductal gray matter, a functional role of this entity in the expression of positive emotions has been postulated.The purpose of the present study was to ascertain whether the deletion of neurons in the parvafox nucleus influenced the tickling-induced 50-kHz calls, which are thought to reflect positive affective states, in rats. To this end, tickling of the animals (heterospecific play) was combined with intracerebral injections of the excitotoxin kainic acid into the parvafox nucleus.The most pronounced surgery-associated reduction in 50-kHz call-numbers was observed in the group of rats in which, on the basis of PV-immunoreactive-cell counts in the parvafox nucleus, bilateral lesions had been successfully produced. Two other parameters that were implemented to quantify positive affective behaviour, namely, an approach towards and a following of the hand of the tickling * Corresponding author at: Institute of Anatomy, University of Fribourg, Rte A. Gockel 1, CH-1700 Fribourg, Switzerland.E-mail address: marco.celio@unifr.ch (M.R. Celio). 1Published in which should be cited to refer to this work.http://doc.rero.ch experimenter, were likewise most markedly suppressed in the group of rats with bilaterally successful lesions. Furthermore, positive correlations were found between each of the investigated parameters. Our data afford evidence that the parvafox nucleus plays a role in the production of 50-kHz calls in rats, and, more generally, in the expression of positive emotions.

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Section: Discussionmentioning

confidence: 95%

Reduction in 50-kHz call-numbers and suppression of tickling-associated positive affective behaviour after lesioning of the lateral hypothalamic parvafox nucleus in rats

Roccaro-Waldmeyer

Babalian

Müller

et al. 2016

Behavioural Brain Research

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“…Recently, Jarvis and collaborators gave evidence that in songbirds and humans very similar networks of cortical-pallial and striatal regions related to vocal learning have evolved, including Broca-and Wernicke-like language centres (cf. [57]). …”

Section: Bird Brainsmentioning

confidence: 99%

Neuronal factors determining high intelligence

Dicke¹,

Roth²

2016

Phil. Trans. R. Soc. B

145

107

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One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Many attempts have been made to correlate degrees of both animal and human intelligence with brain properties. With respect to mammals, a much-discussed trait concerns absolute and relative brain size, either uncorrected or corrected for body size. However, the correlation of both with degrees of intelligence yields large inconsistencies, because although they are regarded as the most intelligent mammals, monkeys and apes, including humans, have neither the absolutely nor the relatively largest brains. The best fit between brain traits and degrees of intelligence among mammals is reached by a combination of the number of cortical neurons, neuron packing density, interneuronal distance and axonal conduction velocity-factors that determine general information processing capacity (IPC), as reflected by general intelligence. The highest IPC is found in humans, followed by the great apes, Old World and New World monkeys. The IPC of cetaceans and elephants is much lower because of a thin cortex, low neuron packing density and low axonal conduction velocity. By contrast, corvid and psittacid birds have very small and densely packed pallial neurons and relatively many neurons, which, despite very small brain volumes, might explain their high intelligence. The evolution of a syntactical and grammatical language in humans most probably has served as an additional intelligence amplifier, which may have happened in songbirds and psittacids in a convergent manner.

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“…With respect to intelligence, among birds, parrots and corvids stand out [90], which interestingly are all vocal learners [46], and among mammals primates stand out [3,55]. Within primates, prosimians exhibit manipulatory, perceptual and cognitive capacities, although often only as a basic ability.…”

Section: Resultsmentioning

confidence: 99%

“…R. Soc. B 370: 20150049 sensory cortex of mammals (see below), N and H to layers 2 and 3 of the secondary mammalian cortex, MV and MD to layers 3 and 6 of the tertiary cortex and AP to layer 5 of the motor cortex and of other cortices [42,[44][45][46].…”

Section: (F ) Birdsmentioning

confidence: 99%

Convergent evolution of complex brains and high intelligence

Roth

2015

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Origin and evolution of the nervous system'. Within the animal kingdom, complex brains and high intelligence have evolved several to many times independently, e.g. among ecdysozoans in some groups of insects (e.g. blattoid, dipteran, hymenopteran taxa), among lophotrochozoans in octopodid molluscs, among vertebrates in teleosts (e.g. cichlids), corvid and psittacid birds, and cetaceans, elephants and primates. High levels of intelligence are invariantly bound to multimodal centres such as the mushroom bodies in insects, the vertical lobe in octopodids, the pallium in birds and the cerebral cortex in primates, all of which contain highly ordered associative neuronal networks. The driving forces for high intelligence may vary among the mentioned taxa, e.g. needs for spatial learning and foraging strategies in insects and cephalopods, for social learning in cichlids, instrumental learning and spatial orientation in birds and social as well as instrumental learning in primates.

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Convergent transcriptional specializations in the brains of humans and song-learning birds

Cited by 420 publications

References 117 publications

Reduction in 50-kHz call-numbers and suppression of tickling-associated positive affective behaviour after lesioning of the lateral hypothalamic parvafox nucleus in rats

Reduction in 50-kHz call-numbers and suppression of tickling-associated positive affective behaviour after lesioning of the lateral hypothalamic parvafox nucleus in rats

Neuronal factors determining high intelligence

Convergent evolution of complex brains and high intelligence

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