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      Amygdala–midbrain connectivity indicates a role for the mammalian parental care system in human altruism

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          Abstract

          <p class="first" id="d4330555e254">Costly altruism benefitting a stranger is a rare but evolutionarily conserved phenomenon. This behaviour may be supported by limbic and midbrain circuitry that supports mammalian caregiving. In rodents, reciprocal connections between the amygdala and the midbrain periaqueductal grey (PAG) are critical for generating protective responses toward vulnerable and distressed offspring. We used functional and structural magnetic resonance imaging to explore whether these regions play a role in supporting costly altruism in humans. We recruited a rare population of altruists, all of whom had donated a kidney to a stranger, and measured activity and functional connectivity of the amygdala and PAG as altruists and matched controls responded to care-eliciting scenarios. When these scenarios were coupled with pre-attentive distress cues, altruists' sympathy corresponded to greater activity in the left amygdala and PAG, and functional connectivity analyses revealed increased coupling between these regions in altruists during this epoch. We also found that altruists exhibited greater fractional anisotropy within the left amygdala–PAG white matter tract. These results, coupled with previous evidence of altruists' increased amygdala-linked sensitivity to distress, are consistent with costly altruism resulting from enhanced care-oriented responses to vulnerability and distress that are supported by recruitment of circuitry that supports mammalian parental care. </p>

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          Most cited references55

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          Oxytocin modulates neural circuitry for social cognition and fear in humans.

          In non-human mammals, the neuropeptide oxytocin is a key mediator of complex emotional and social behaviors, including attachment, social recognition, and aggression. Oxytocin reduces anxiety and impacts on fear conditioning and extinction. Recently, oxytocin administration in humans was shown to increase trust, suggesting involvement of the amygdala, a central component of the neurocircuitry of fear and social cognition that has been linked to trust and highly expresses oxytocin receptors in many mammals. However, no human data on the effects of this peptide on brain function were available. Here, we show that human amygdala function is strongly modulated by oxytocin. We used functional magnetic resonance imaging to image amygdala activation by fear-inducing visual stimuli in 15 healthy males after double-blind crossover intranasal application of placebo or oxytocin. Compared with placebo, oxytocin potently reduced activation of the amygdala and reduced coupling of the amygdala to brainstem regions implicated in autonomic and behavioral manifestations of fear. Our results indicate a neural mechanism for the effects of oxytocin in social cognition in the human brain and provide a methodology and rationale for exploring therapeutic strategies in disorders in which abnormal amygdala function has been implicated, such as social phobia or autism.
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            A neural basis for social cooperation.

            Cooperation based on reciprocal altruism has evolved in only a small number of species, yet it constitutes the core behavioral principle of human social life. The iterated Prisoner's Dilemma Game has been used to model this form of cooperation. We used fMRI to scan 36 women as they played an iterated Prisoner's Dilemma Game with another woman to investigate the neurobiological basis of cooperative social behavior. Mutual cooperation was associated with consistent activation in brain areas that have been linked with reward processing: nucleus accumbens, the caudate nucleus, ventromedial frontal/orbitofrontal cortex, and rostral anterior cingulate cortex. We propose that activation of this neural network positively reinforces reciprocal altruism, thereby motivating subjects to resist the temptation to selfishly accept but not reciprocate favors.
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              Midbrain circuits for defensive behaviour.

              Survival in threatening situations depends on the selection and rapid execution of an appropriate active or passive defensive response, yet the underlying brain circuitry is not understood. Here we use circuit-based optogenetic, in vivo and in vitro electrophysiological, and neuroanatomical tracing methods to define midbrain periaqueductal grey circuits for specific defensive behaviours. We identify an inhibitory pathway from the central nucleus of the amygdala to the ventrolateral periaqueductal grey that produces freezing by disinhibition of ventrolateral periaqueductal grey excitatory outputs to pre-motor targets in the magnocellular nucleus of the medulla. In addition, we provide evidence for anatomical and functional interaction of this freezing pathway with long-range and local circuits mediating flight. Our data define the neuronal circuitry underlying the execution of freezing, an evolutionarily conserved defensive behaviour, which is expressed by many species including fish, rodents and primates. In humans, dysregulation of this 'survival circuit' has been implicated in anxiety-related disorders.

                Author and article information

                Journal
                Proceedings of the Royal Society B: Biological Sciences
                Proc. R. Soc. B
                The Royal Society
                0962-8452
                1471-2954
                October 25 2017
                October 25 2017
                : 284
                : 1865
                : 20171731
                Article
                10.1098/rspb.2017.1731
                5666102
                29070724
                395a0f3d-7803-4af2-90f1-9d27580924d5
                © 2017

                http://royalsocietypublishing.org/licence

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