Helping Behavior in Prairie Voles: A Model of Empathy and the Importance of Oxytocin

Kitano, Kota; Yamagishi, Atsuhito; Horie, Katsutoshi; Nishimori, Katsuhiko; Sato, Nobuya

doi:10.1101/2020.10.20.347872

Cited by 2 publications

(3 citation statements)

References 68 publications

(123 reference statements)

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“…Many cortical areas displayed sparse labeling of Oxtr mRNA, but some, including the anterior cingulate and insular cortices, showed strong labeling in restricted layers, primarily layers two, five, and six. Oxytocin signaling in the anterior cingulate cortex is critical for consoling and helping behaviors in prairie voles (Burkett et al., 2016; Kitano et al., 2020), mandarin voles (L. F. Li et al., 2020), and rats (Yamagishi et al., 2020). In the insular cortex, OXTR activity is necessary for rats to demonstrate appropriate social affective preference, that is, to approach stressed juveniles and avoid stressed adults (Rogers‐Carter et al., 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Oxytocin signaling in the anterior cingulate cortex is critical for consoling and helping behaviors in prairie voles (Burkett et al, 2016;Kitano et al, 2020), mandarin voles (L. F. Li et al, 2020), and rats (Yamagishi et al, 2020). In the insular cortex, OXTR activity is necessary for rats to demonstrate appropriate social affective preference, that is, to approach stressed juveniles and avoid stressed adults (Rogers-Carter et al, 2018).…”

Section: Oxytocin Receptor Mrna Expression In Select Areas Influencin...mentioning

confidence: 99%

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Oxytocin receptors are widely distributed in the prairie vole (Microtus ochrogaster) brain: Relation to social behavior, genetic polymorphisms, and the dopamine system

Inoue

Ford

Horie

et al. 2022

J of Comparative Neurology

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Oxytocin regulates social behavior via direct modulation of neurons, regulation of neural network activity, and interaction with other neurotransmitter systems. The behavioral effects of oxytocin signaling are determined by the species‐specific distribution of brain oxytocin receptors. The socially monogamous prairie vole has been a useful model organism for elucidating the role of oxytocin in social behaviors, including pair bonding, response to social loss, and consoling. However, there has been no comprehensive mapping of oxytocin receptor‐expressing cells throughout the prairie vole brain. Here, we employed a highly sensitive in situ hybridization, RNAscope, to construct an exhaustive, brain‐wide map of oxytocin receptor mRNA‐expressing cells. We found that oxytocin receptor mRNA expression was widespread and diffused throughout the brain, with specific areas displaying a particularly robust expression. Comparing receptor binding with mRNA revealed that regions of the hippocampus and substantia nigra contained oxytocin receptor protein but lacked mRNA, indicating that oxytocin receptors can be transported to distal neuronal processes, consistent with presynaptic oxytocin receptor functions. In the nucleus accumbens, a region involved in oxytocin‐dependent social bonding, oxytocin receptor mRNA expression was detected in both the D1 and D2 dopamine receptor‐expressing subtypes of cells. Furthermore, natural genetic polymorphisms robustly influenced oxytocin receptor expression in both D1 and D2 receptor cell types in the nucleus accumbens. Collectively, our findings further elucidate the extent to which oxytocin signaling is capable of influencing brain‐wide neural activity, responses to social stimuli, and social behavior. Key points Oxytocin receptor mRNA is diffusely expressed throughout the brain, with strong expression concentrated in certain areas involved in social behavior. Oxytocin receptor mRNA expression and protein localization are misaligned in some areas, indicating that the receptor protein may be transported to distal processes. In the nucleus accumbens, oxytocin receptors are expressed on cells expressing both D1 and D2 dopamine receptor subtypes, and the majority of variation in oxytocin receptor expression between animals is attributable to polymorphisms in the oxytocin receptor gene.

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Section: Discussionmentioning

confidence: 99%

Section: Oxytocin Receptor Mrna Expression In Select Areas Influencin...mentioning

confidence: 99%

Oxytocin receptors are widely distributed in the prairie vole (Microtus ochrogaster) brain: Relation to social behavior, genetic polymorphisms, and the dopamine system

Inoue

Ford

Horie

et al. 2022

J of Comparative Neurology

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“…Furthermore, both in zebrafish and in rodents oxytocin also regulates emotion recognition [23,26], which is the cognitive basis for emotion contagion. Therefore, it is plausible that oxytocin has been recruited early in the evolution of nonapeptides to regulate ancestral empathic behaviors in group living species, and that it has been evolutionary co-opted to regulate more complex empathic behaviors, such as consolation and helping [24,[27][28][29][30], in species with more complex cognitive abilities. From a translational research perspective our results provide content and construct validity to a phylogenetically distant model of emotional contagion.…”

Section: Main Textmentioning

confidence: 99%

Oxytocin regulation of social transmission of fear in zebrafish reveals its evolutionary conserved role in emotional contagion

Akinrinade

Kareklas

Gliksberg

et al. 2021

Preprint

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Emotional contagion is the most ancestral form of empathy that relies on simple perception-action mechanisms, on top of which more complex forms of empathic behaviors, such as consolation and helping, have evolved. Here we tested to what extent the proximate mechanisms of emotional contagion are evolutionary conserved by assessing the role of oxytocin, known to regulate empathic behaviors in mammals, in social fear contagion in zebrafish, which represents an evolutionary divergent line to that of tetrapods, within vertebrates. Using mutants for the ligand of the fish oxytocin nonapeptide and both of its receptors in zebrafish we showed that oxytocin is necessary for observer zebrafish to copy the distressed behavior of conspecific demonstrators. Exogeneous administration of oxytocin to the ligand mutant rescued the ability of observers to express social fear transmission, indicating that oxytocin is not only necessary but also sufficient for emotional contagion. The brain regions in the ventral telencephalon that are associated with emotional contagion in zebrafish are homologous to those known to be involved in the same process in rodents (e.g. striatum, lateral septum), and receive direct projections from oxytocinergic neurons located in the preoptic area. Finally, we ruled out the hypothesis that social transmission of fear in zebrafish merely relies on behavior contagion by motor imitation, and we showed that it rather relies on emotion discrimination. Together our results support an evolutionary conserved role for oxytocin as a key regulator of basic empathic behaviors across vertebrates.

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Helping Behavior in Prairie Voles: A Model of Empathy and the Importance of Oxytocin

Cited by 2 publications

References 68 publications

Oxytocin receptors are widely distributed in the prairie vole (Microtus ochrogaster) brain: Relation to social behavior, genetic polymorphisms, and the dopamine system

Oxytocin receptors are widely distributed in the prairie vole (Microtus ochrogaster) brain: Relation to social behavior, genetic polymorphisms, and the dopamine system

Oxytocin regulation of social transmission of fear in zebrafish reveals its evolutionary conserved role in emotional contagion

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