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      Evolution of Pallial Areas and Networks Involved in Sociality: Comparison Between Mammals and Sauropsids

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          Abstract

          Birds are extremely interesting animals for studying the neurobiological basis of cognition and its evolution. They include species that are highly social and show high cognitive capabilities. Moreover, birds rely more on visual and auditory cues than on olfaction for social behavior and cognition, just like primates. In primates, there are two major brain networks associated to sociality: (1) one related to perception and decision-making, involving the pallial amygdala (with the basolateral complex as a major component), the temporal and temporoparietal neocortex, and the orbitofrontal cortex; (2) another one related to affiliation, including the medial extended amygdala, the ventromedial prefrontal and anterior cingulate cortices, the ventromedial striatum (largely nucleus accumbens), and the ventromedial hypothalamus. In this account, we used an evolutionary developmental neurobiology approach, in combination with published comparative connectivity and functional data, to identify areas and functional networks in the sauropsidian brain comparable to those of mammals that are related to decision-making and affiliation. Both in mammals and sauropsids, there is an important interaction between these networks by way of cross projections between areas of both systems.

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          Most cited references114

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          Oxytocin, vasopressin, and the neurogenetics of sociality.

          There is growing evidence that the neuropeptides oxytocin and vasopressin modulate complex social behavior and social cognition. These ancient neuropeptides display a marked conservation in gene structure and expression, yet diversity in the genetic regulation of their receptors seems to underlie natural variation in social behavior, both between and within species. Human studies are beginning to explore the roles of these neuropeptides in social cognition and behavior and suggest that variation in the genes encoding their receptors may contribute to variation in human social behavior by altering brain function. Understanding the neurobiology and neurogenetics of social cognition and behavior has important implications, both clinically and for society.
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            The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.

            The human orbitofrontal cortex is an important brain region for the processing of rewards and punishments, which is a prerequisite for the complex and flexible emotional and social behaviour which contributes to the evolutionary success of humans. Yet much remains to be discovered about the functions of this key brain region, and new evidence from functional neuroimaging and clinical neuropsychology is affording new insights into the different functions of the human orbitofrontal cortex. We review the neuroanatomical and neuropsychological literature on the human orbitofrontal cortex, and propose two distinct trends of neural activity based on a meta-analysis of neuroimaging studies. One is a mediolateral distinction, whereby medial orbitofrontal cortex activity is related to monitoring the reward value of many different reinforcers, whereas lateral orbitofrontal cortex activity is related to the evaluation of punishers which may lead to a change in ongoing behaviour. The second is a posterior-anterior distinction with more complex or abstract reinforcers (such as monetary gain and loss) represented more anteriorly in the orbitofrontal cortex than simpler reinforcers such as taste or pain. Finally, we propose new neuroimaging methods for obtaining further evidence on the localisation of function in the human orbitofrontal cortex.
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              Social reward requires coordinated activity of accumbens oxytocin and 5HT

              Social behaviors in species as diverse as honey bees and humans promote group survival but often come at some cost to the individual. Although reinforcement of adaptive social interactions is ostensibly required for the evolutionary persistence of these behaviors, the neural mechanisms by which social reward is encoded by the brain are largely unknown. Here we demonstrate that in mice oxytocin (OT) acts as a social reinforcement signal within the nucleus accumbens (NAc) core, where it elicits a presynaptically expressed long-term depression of excitatory synaptic transmission in medium spiny neurons. Although the NAc receives OT receptor-containing inputs from several brain regions, genetic deletion of these receptors specifically from dorsal raphe nucleus, which provides serotonergic (5-HT) innervation to the NAc, abolishes the reinforcing properties of social interaction. Furthermore, OT-induced synaptic plasticity requires activation of NAc 5-HT1b receptors, the blockade of which prevents social reward. These results demonstrate that the rewarding properties of social interaction in mice require the coordinated activity of OT and 5-HT in the NAc, a mechanistic insight with implications for understanding the pathogenesis of social dysfunction in neuropsychiatric disorders such as autism.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                12 July 2019
                2019
                : 10
                : 894
                Affiliations
                Department of Experimental Medicine, Institut de Recerca Biomèdica de Lleida - Fundació Dr. Pifarré (IRBLleida), University of Lleida , Lleida, Spain
                Author notes

                Edited by: Andras Csillag, Semmelweis University, Hungary

                Reviewed by: Enrique Lanuza, University of Valencia, Spain; Fernando Garcia-Moreno, Achucarro Basque Center for Neuroscience, Spain

                *Correspondence: Loreta Medina, loreta.medina@ 123456mex.udl.cat

                This article was submitted to Avian Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2019.00894
                6640085
                2c624a1a-bdbd-482c-8248-0c9e18494ba1
                Copyright © 2019 Medina, Abellán and Desfilis.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 March 2019
                : 27 June 2019
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 133, Pages: 15, Words: 13743
                Funding
                Funded by: Spanish Ministerio de Economía y Competitividad (MINECO)
                Funded by: Fondo Europeo de Desarrollo Regional (FEDER) 10.13039/501100008530
                Award ID: BFU2015-68537-R
                Categories
                Physiology
                Hypothesis and Theory

                Anatomy & Physiology
                medial amygdala,bst,social cognition,affiliation,dorsal ventricular ridge,six part pallial model,orbito frontal cortex,pallial amygdala

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