Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Growing a social brain

An Author Correction to this article was published on 22 August 2018

This article has been updated

Abstract

It has long been assumed that social animals, such as humans, are born with a brain system that has evolved to support social affiliation. However, the evidence does not necessarily support this assumption. Alternatively, social animals can be defined as those who cannot survive alone and rely on members from their group to regulate their ongoing physiology (or allostasis). The rather simple evolutionary constraint of social dependency for survival can be sufficient to make the social environment vitally salient, and to provide the ultimate driving force for socially crafted brain development and learning. In this Perspective, we propose a framework for sociality and specify a set of hypotheses on the mechanisms of social development and underlying neural systems. The theoretical shift proposed here implies that profound human characteristics, including but not limited to sociality, are acquired at an early age, while social interactions provide key wiring instructions that determine brain development.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Growing a social brain.
Fig. 2: The anterior insula is a hub that integrates exteroceptive to interoceptive inputs.
Fig. 3: Concepts as predictions.
Fig. 4: Relationship between allostasis, concepts and social development.

Change history

  • 22 August 2018

    In the version of this Perspective originally published, at the end of the first paragraph of the section ‘Neural prediction as a potential mechanism for how experience sculpts the developing brain’ the citation to ref. 76 should have been to ref. 74, and at the end of the first sentence of the next paragraph ref. 76 should have been cited alongside ref. 74. These have now been corrected.

References

  1. Rand, D. G. & Nowak, M. A. Human cooperation. Trends Cogn. Sci. 17, 413–425 (2013).

    Article  PubMed  Google Scholar 

  2. Johnson, Z. V. & Young, L. J. Neurobiological mechanisms of social attachment and pair bonding. Curr. Opin. Behav. Sci. 3, 38–44 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Hawkes, K. Grandmothers and the evolution of human longevity. Am. J. Hum. Biol. 15, 380–400 (2003).

    Article  PubMed  Google Scholar 

  4. Dunbar, R. I. & Shultz, S. Evolution in the social brain. Science 317, 1344–1347 (2007).

    Article  CAS  PubMed  Google Scholar 

  5. Sterling, P. Allostasis: a model of predictive regulation. Physiol. Behav. 106, 5–15 (2012).

    Article  CAS  PubMed  Google Scholar 

  6. Atzil, S. & Barrett, L. F. Social regulation of allostasis: Commentary on “Mentalizing homeostasis: the social origins of interoceptive inference” by Fotopoulou & Tsakiris. Neuropsychoanalysis 19, 1–24 (2017).

    Article  Google Scholar 

  7. Rao, P. N. S., Shashidhar, A. & Ashok, C. In utero fuel homeostasis: lessons for a clinician. Indian J. Endocrinol. Metab. 17, 60–68 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Winberg, J. Mother and newborn baby: mutual regulation of physiology and behavior — a selective review. Dev. Psychobiol. 47, 217–229 (2005).

    Article  PubMed  Google Scholar 

  9. Hofer, M. A. Hidden regulators in attachment, separation, and loss. Monogr. Soc. Res. Child Dev. 59, 192–207 (1994).

    Article  CAS  PubMed  Google Scholar 

  10. Feldman, R., Magori-Cohen, R., Galili, G., Singer, M. & Louzoun, Y. Mother and infant coordinate heart rhythms through episodes of interaction synchrony. Infant Behav. Dev. 34, 569–577 (2011).

    Article  PubMed  Google Scholar 

  11. Feldman, R., Eidelman, A. I., Sirota, L. & Weller, A. Comparison of skin-to-skin (kangaroo) and traditional care: parenting outcomes and preterm infant development. Pediatrics 110, 16–26 (2002).

    Article  PubMed  Google Scholar 

  12. Keramati, M. & Gutkin, B. Homeostatic reinforcement learning for integrating reward collection and physiological stability. eLife 3, e04811 (2014).

    Article  PubMed Central  Google Scholar 

  13. Barrett, L. F. & Satpute, A. B. Large-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain. Curr. Opin. Neurobiol. 23, 361–372 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kleckner, I. et al. Evidence for a large-scale brain system supporting allostasis and interoception in humans. Nat. Hum. Behav. 1, 0069 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Barrett, L. F. How Emotions are Made (Houghton Mifflin Harcourt, Boston, MA, 2017).

  16. Gao, W., Lin, W., Grewen, K. & Gilmore, J. H. Functional connectivity of the infant human brain plastic and modifiable. Neuroscientist 23, 169–184 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bullmore, E. & Sporns, O. The economy of brain network organization. Nat. Rev. Neurosci. 13, 336–349 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Yeo, B. T. et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125–1165 (2011).

    Article  PubMed  Google Scholar 

  19. van den Heuvel, M. P. & Sporns, O. Rich-club organization of the human connectome. J. Neurosci. 31, 15775–15786 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. van den Heuvel, M. P. et al. Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70, 783–792 (2013).

    Article  PubMed  Google Scholar 

  21. Atzil, S., Hendler, T. & Feldman, R. Specifying the neurobiological basis of human attachment: brain, hormones, and behavior in synchronous and intrusive mothers. Neuropsychopharmacology 36, 2603–2615 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Atzil, S., Hendler, T. & Feldman, R. The brain basis of social synchrony. Soc. Cogn. Affect. Neurosci. 9, 1193–1202 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Atzil, S. et al. Dopamine in the medial amygdala network mediates human bonding. Proc. Natl Acad. Sci. USA 114, 2361–2366 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bickart, K. C., Hollenbeck, M. C., Barrett, L. F. & Dickerson, B. C. Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. J. Neurosci. 32, 14729–14741 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Uddin, L. Q. et al. Salience network–based classification and prediction of symptom severity in children with autism. JAMA Psychiatry 70, 869–879 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Di Martino, A. et al. The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol. Psychiatry 19, 659–667 (2014).

    Article  PubMed  Google Scholar 

  27. Dubois, J. et al. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276, 48–71 (2014).

    Article  CAS  PubMed  Google Scholar 

  28. Gao, W. et al. Temporal and spatial evolution of brain network topology during the first two years of life. PLoS ONE 6, e25278 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gao, W. et al. The synchronization within and interaction between the default and dorsal attention networks in early infancy. Cereb. Cortex 23, 594–603 (2013).

    Article  PubMed  Google Scholar 

  30. Gao, W. et al. Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. Am. J. Neuroradiol. 30, 290–296 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Smyser, C. D., Snyder, A. Z. & Neil, J. J. Functional connectivity MRI in infants: exploration of the functional organization of the developing brain. Neuroimage 56, 1437–1452 (2011).

    Article  PubMed  Google Scholar 

  32. Fransson, P., Aden, U., Blennow, M. & Lagercrantz, H. The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb. Cortex 21, 145–154 (2011).

    Article  PubMed  Google Scholar 

  33. Fransson, P. et al. Resting-state networks in the infant brain. Proc. Natl Acad. Sci. USA 104, 15531–15536 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Elton, A., Alcauter, S. & Gao, W. Network connectivity abnormality profile supports a categorical-dimensional hybrid model of ADHD. Hum. Brain Mapp. 35, 4531–4543 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Fair, D. A. et al. The maturing architecture of the brain's default network. Proc. Natl Acad. Sci. USA 105, 4028–4032 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tau, G. Z. & Peterson, B. S. Normal development of brain circuits. Neuropsychopharmacology 35, 147–168 (2010).

    Article  PubMed  Google Scholar 

  37. Stiles, J. & Jernigan, T. L. The basics of brain development. Neuropsychol. Rev. 20, 327–348 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Dubois, J. et al. Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131, 2028–2041 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Finlay, B. L. & Uchiyama, R. in Evolution of Nervous Systems 2nd edn (ed. Kaas, J. H.) 123–148 (Elsevier, Oxford, 2017).

  40. Rogers, C. E. et al. Regional cerebral development at term relates to school-age social-emotional development in very preterm children. J. Am. Acad. Child Adolesc. Psychiatry 51, 181–191 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Woodward, L. J., Clark, C. A., Bora, S. & Inder, T. E. Neonatal white matter abnormalities an important predictor of neurocognitive outcome for very preterm children. PLoS ONE 7, e51879 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Curley, J. P. & Champagne, F. A. Influence of maternal care on the developing brain: mechanisms, temporal dynamics and sensitive periods. Front. Neuroendocrinol. 40, 52–66 (2016).

    Article  PubMed  Google Scholar 

  43. Johnson, M. H. Functional brain development in humans. Nat. Rev. Neurosci. 2, 475–483 (2001).

    Article  CAS  PubMed  Google Scholar 

  44. Feldman, R. Parent–infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. J. Child Psychol. Psychiatry 48, 329–354 (2007).

    Article  PubMed  Google Scholar 

  45. Tomoda, A. et al. Reduced prefrontal cortical gray matter volume in young adults exposed to harsh corporal punishment. Neuroimage 47, T66–T71 (2009).

    Article  PubMed  Google Scholar 

  46. Whittle, S. et al. Positive parenting predicts the development of adolescent brain structure: a longitudinal study. Dev. Cogn. Neurosci. 8, 7–17 (2014).

    Article  PubMed  Google Scholar 

  47. Teicher, M. H., Anderson, C. M. & Polcari, A. Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc. Natl Acad. Sci. USA 109, E563–E572 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Luby, J. L. et al. Maternal support in early childhood predicts larger hippocampal volumes at school age. Proc. Natl Acad. Sci. USA 109, 2854–2859 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Champagne, F. A. et al. Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology 147, 2909–2915 (2006).

    Article  CAS  PubMed  Google Scholar 

  50. McGowan, P. O. et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12, 342–348 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pena, C. J., Neugut, Y. D., Calarco, C. A. & Champagne, F. A. Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring. Eur. J. Neurosci. 39, 946–956 (2014).

    Article  PubMed  Google Scholar 

  52. Insel, T. R. Oxytocin — a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 17, 3–35 (1992).

    Article  CAS  PubMed  Google Scholar 

  53. Webb, A. R., Heller, H. T., Benson, C. B. & Lahav, A. Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation. Proc. Natl Acad. Sci. USA 112, 3152–3157 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Teicher, M. H., Samson, J. A., Anderson, C. M. & Ohashi, K. The effects of childhood maltreatment on brain structure, function and connectivity. Nat. Rev. Neurosci. 17, 652–666 (2016).

    Article  CAS  PubMed  Google Scholar 

  55. Suomi, S. J. Early determinants of behaviour: evidence from primate studies. Br. Med. Bull. 53, 170–184 (1997).

    Article  CAS  PubMed  Google Scholar 

  56. Arling, G. L. & Harlow, H. F. Effects of social deprivation on maternal behavior of rhesus monkeys. J. Comp. Physiol. Psychol. 64, 371–377 (1967).

    Article  CAS  PubMed  Google Scholar 

  57. Harlow, H. F. Total social isolation: effects on macaque monkey behavior. Science 148, 666 (1965).

    Article  CAS  PubMed  Google Scholar 

  58. Champagne, F. A., Francis, D. D., Mar, A. & Meaney, M. J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 79, 359–371 (2003).

    Article  CAS  PubMed  Google Scholar 

  59. Champagne, F. A. Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 29, 386–397 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Champagne, F. & Meaney, M. J. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog. Brain Res. 133, 287–302 (2001).

    Article  CAS  PubMed  Google Scholar 

  61. Pena, C. J., Neugut, Y. D. & Champagne, F. A. Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology 154, 4340–4351 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Feldman, R. The adaptive human parental brain: implications for children’s social development. Trends Neurosci. 38, 387–399 (2015).

    Article  CAS  PubMed  Google Scholar 

  63. Granat, A., Gadassi, R., Gilboa-Schechtman, E. & Feldman, R. Maternal depression and anxiety, social synchrony, and infant regulation of negative and positive emotions. Emotion 17, 11–27 (2016).

    Article  PubMed  Google Scholar 

  64. Herba, C. M. Maternal depression and child behavioural outcomes. Lancet Psychiatry 1, 408–409 (2014).

    Article  PubMed  Google Scholar 

  65. Raby, K. L., Roisman, G. I., Simpson, J. A., Collins, W. A. & Steele, R. D. Greater maternal insensitivity in childhood predicts greater electrodermal reactivity during conflict discussions with romantic partners in adulthood. Psychol. Sci. 26, 348–353 (2015).

    Article  PubMed  Google Scholar 

  66. Feldman, R. Parent–infant synchrony: biological foundations and developmental outcomes. Curr. Dir. Psychol. Sci. 16, 340–345 (2007).

    Article  Google Scholar 

  67. Carey, S. & Spelke, E. Science and core knowledge. Philos. Sci. 63, 515–533 (1996).

    Article  Google Scholar 

  68. Spelke, E. S. & Kinzler, K. D. Core knowledge. Dev. Sci. 10, 89–96 (2007).

    Article  PubMed  Google Scholar 

  69. Clark, A. Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behav. Brain Sci. 36, 181–204 (2013).

    Article  PubMed  Google Scholar 

  70. Hohwy, J. The Predictive Mind (Oxford Univ. Press, Oxford, 2013).

  71. Rao, R. P. & Ballard, D. H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2, 79–87 (1999).

    Article  CAS  PubMed  Google Scholar 

  72. Friston, K. The free-energy principle: a unified brain theory? Nat. Rev. Neurosci. 11, 127–138 (2010).

    Article  CAS  PubMed  Google Scholar 

  73. Clark, A. Are we predictive engines? Perils, prospects, and the puzzle of the porous perceiver. Behav. Brain Sci. 36, 233–253 (2013).

    Article  PubMed  Google Scholar 

  74. Barrett, L. F. & Simmons, W. K. Interoceptive predictions in the brain. Nat. Rev. Neurosci. 16, 419–429 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Chanes, L. & Barrett, L. F. Redefining the role of limbic areas in cortical processing. Trends Cogn. Sci. 20, 96–106 (2016).

    Article  PubMed  Google Scholar 

  76. Friston, K. A theory of cortical responses. Philos. Trans. R. Soc. London Ser. B 360, 815–836 (2005).

    Article  Google Scholar 

  77. Gopnik, A. The Philosophical Baby (Bodley Head, London, 2009).

    Google Scholar 

  78. Siegelman, N. & Frost, R. Statistical learning as an individual ability: theoretical perspectives and empirical evidence. J. Mem. Lang. 81, 105–120 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Krogh, L., Vlach, H. A. & Johnson, S. P. Statistical learning across development: flexible yet constrained. Front. Psychol. 3, 598 (2012).

    Article  PubMed  Google Scholar 

  80. Saffran, J. R., Aslin, R. N. & Newport, E. L. Statistical learning by 8-month-old infants. Science 274, 1926–1928 (1996).

    Article  CAS  PubMed  Google Scholar 

  81. Kirkham, N. Z., Slemmer, J. A. & Johnson, S. P. Visual statistical learning in infancy: evidence for a domain general learning mechanism. Cognition 83, B35–B42 (2002).

    Article  PubMed  Google Scholar 

  82. Tenenbaum, J. B., Kemp, C., Griffiths, T. L. & Goodman, N. D. How to grow a mind: statistics, structure, and abstraction. Science 331, 1279–1285 (2011).

    Article  CAS  PubMed  Google Scholar 

  83. Sterling, P. & Laughlin, S. Principles of Neural Design (MIT Press, Cambridge, MA, 2015).

  84. Carpenter, R. Homeostasis: a plea for a unified approach. Adv. Physiol. Educ. 28, 180–187 (2004).

    Article  CAS  PubMed  Google Scholar 

  85. Gu, X. & FitzGerald, T. Interoceptive inference: homeostasis and decision-making. Trends Cogn. Sci. 18, 269–270 (2014).

    Article  PubMed  Google Scholar 

  86. Seth, A. K. Interoceptive inference, emotion, and the embodied self. Trends Cogn. Sci. 17, 565–573 (2013).

    Article  PubMed  Google Scholar 

  87. Seth, A. K., Suzuki, K. & Critchley, H. D. An interoceptive predictive coding model of conscious presence. Front. Psychol. 2, 395 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Finlay, B. L. & Syal, S. The pain of altruism. Trends Cogn. Sci. 18, 615–617 (2014).

    Article  PubMed  Google Scholar 

  89. Lummaa, V., Vuorisalo, T., Barr, R. G. & Lehtonen, L. Why cry? Adaptive significance of intensive crying in human infants. Evol. Hum. Behav. 19, 193–202 (1998).

    Article  Google Scholar 

  90. Davis, E. P. et al. Exposure to unpredictable maternal sensory signals influences cognitive development across species. Proc. Natl Acad. Sci. USA 114, 10390–10395 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Stein, B. E., Stanford, T. R. & Rowland, B. A. Development of multisensory integration from the perspective of the individual neuron. Nat. Rev. Neurosci. 15, 520–535 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Petanjek, Z., Judaš, M., Kostović, I. & Uylings, H. B. M. Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. Cereb. Cortex 18, 915–929 (2008).

    Article  PubMed  Google Scholar 

  93. Alcauter, S. et al. Development of thalamocortical connectivity during infancy and its cognitive correlations. J. Neurosci. 34, 9067–9075 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Alcauter, S., Lin, W., Keith Smith, J., Gilmore, J. H. & Gao, W. Consistent anterior-posterior segregation of the insula during the first 2 years of life. Cereb. Cortex 25, 1176–1187 (2015).

    Article  PubMed  Google Scholar 

  95. Trachtenberg, J. T. & Stryker, M. P. Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J. Neurosci. 21, 3476–3482 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Singer, T. & Lamm, C. The social neuroscience of empathy. Ann. N. Y. Acad. Sci. 1156, 81–96 (2009).

    Article  PubMed  Google Scholar 

  97. Andrews-Hanna, J. R., Smallwood, J. & Spreng, R. N. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann. N. Y. Acad. Sci. 1316, 29–52 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Shamay-Tsoory, S. G. The neural bases for empathy. Neuroscientist 17, 18–24 (2011).

    Article  PubMed  Google Scholar 

  99. Ganzel, B. L., Morris, P. A. & Wethington, E. Allostasis and the human brain: integrating models of stress from the social and life sciences. Psychol. Rev. 117, 134–174 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Bickart, K. C., Dickerson, B. C. & Barrett, L. F. The amygdala as a hub in brain networks that support social life. Neuropsychologia 63, 235–248 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).

    Article  CAS  PubMed  Google Scholar 

  102. Lindquist, K. A., Satpute, A. B., Wager, T. D., Weber, J. & Barrett, L. F. The brain basis of positive and negative affect: evidence from a meta-analysis of the human neuroimaging literature. Cereb. Cortex 26, 1910–1922 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  103. Bar, M. The proactive brain: memory for predictions. Philos. Trans. R. Soc. London Ser. B 364, 1235–1243 (2009).

    Article  Google Scholar 

  104. Bar, M. Predictions: a universal principle in the operation of the human brain. Introduction. Philos. Trans. R. Soc. London Ser. B 364, 1181–1182 (2009).

    Article  Google Scholar 

  105. Murphy, G. The Big Book of Concepts (MIT Press, Cambridge, MA, 2004).

  106. Barsalou, L. W. Ad hoc categories. Mem. Cogn. 11, 211–227 (1983).

    Article  CAS  Google Scholar 

  107. Barsalou, L. W., Kyle Simmons, W., Barbey, A. K. & Wilson, C. D. Grounding conceptual knowledge in modality-specific systems. Trends Cogn. Sci. 7, 84–91 (2003).

    Article  PubMed  Google Scholar 

  108. Hollerman, J. R. & Schultz, W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1, 304–309 (1998).

    Article  CAS  PubMed  Google Scholar 

  109. Barrett, L. F. The theory of constructed emotion: an active inference account of interoception and categorization. Soc. Cogn. Affect. Neurosci. 12, 1–23 (2017).

    PubMed  Google Scholar 

  110. Feldman, R., Rosenthal, Z. & Eidelman, A. I. Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biol. Psychiatry 75, 56–64 (2014).

    Article  PubMed  Google Scholar 

  111. Levin, B. E. Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos. Trans. R. Soc. London Ser. B 361, 1107–1121 (2006).

    Article  CAS  Google Scholar 

  112. Bauman, D. in Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction (eds Dobson, A. & Dobson, M. J.) 238–256 (Comstock Publishing Associates, Ithaca, NY, 2000).

  113. Arrieta, M. C., Stiemsma, L. T., Amenyogbe, N., Brown, E. M. & Finlay, B. The intestinal microbiome in early life: health and disease. Front. Immunol. 5, 427 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Nakata, T. & Trehub, S. E. Infants’ responsiveness to maternal speech and singing. Infant Behav. Dev. 27, 455–464 (2004).

    Article  Google Scholar 

  115. Tomasello, M. in Joint Attention: Its Origins and Role in Development (eds ​Moore, C. & Dunham, P.) 103–130 (Psychology Press, New York, NY, 1995).

  116. Amso, D. & Scerif, G. The attentive brain: insights from developmental cognitive neuroscience. Nat. Rev. Neurosci. 16, 606–619 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Baron-Cohen, S. The development of a theory of mind in autism: deviance and delay? Psychiatry Clin. North Am. 14, 33–51 (1991).

    Article  CAS  Google Scholar 

  118. Belmonte, M. K. et al. Autism as a disorder of neural information processing: directions for research and targets for therapy. Mol. Psychiatry 9, 646–663 (2004).

    Article  CAS  PubMed  Google Scholar 

  119. Trehub, S. E. & Gudmundsdottir, H. R. in The Oxford Handbook of Singing (eds Welch, G. & Sergeant, D.) 1–20 (Oxford Univ. Press, Oxford, 2015).

  120. MacLean, P. C. et al. Mother–infant mutual eye gaze supports emotion regulation in infancy during the still-face paradigm. Infant Behav. Dev. 37, 512–522 (2014).

    Article  PubMed  Google Scholar 

  121. Mantis, I., Stack, D. M., Ng, L., Serbin, L. A. & Schwartzman, A. E. Mutual touch during mother–infant face-to-face still-face interactions: influences of interaction period and infant birth status. Infant Behav. Dev. 37, 258–267 (2014).

    Article  PubMed  Google Scholar 

  122. Ramsay, D. S. & Woods, S. C. Clarifying the roles of homeostasis and allostasis in physiological regulation. Psychol. Rev. 121, 225 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  123. Muenzinger, K. F. & Fletcher, F. M. Motivation in learning. VI. Escape from electric shock compared with hunger-food tension in the visual discrimination habit. J. Comp. Psychol. 22, 79 (1936).

    Article  Google Scholar 

  124. Petrinovich, L. & Bolles, R. Deprivation states and behavioral attributes. J. Comp. Physiol. Psychol. 47, 450 (1954).

    Article  CAS  PubMed  Google Scholar 

  125. Okanoya, K. in Evolution of the Brain, Cognition, and Emotion in Vertebrates (eds Watanabe, S., Hofman, M. A. & Shimizu, T.) 207–224 (Springer, Tokyo, 2017).

  126. Scott, J. P. Critical periods in the development of social behavior in puppies. Psychosom. Med. 20, 42–54 (1958).

    Article  CAS  PubMed  Google Scholar 

  127. Li, S. S. Y. & McNally, G. P. The conditions that promote fear learning: prediction error and Pavlovian fear conditioning. Neurobiol. Learn. Mem. 108, 14–21 (2014).

    Article  PubMed  Google Scholar 

  128. Preuss, T. M. The human brain: rewired and running hot. Ann. N. Y. Acad. Sci. 1225, 182–191 (2011).

    Article  Google Scholar 

  129. Spocter, M. A. et al. Neuropil distribution in the cerebral cortex differs between humans and chimpanzees. J. Comp. Neurol. 520, 2917–2929 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  130. Barrett, L. F. The theory of constructed emotion: an active inference account of interoception and categorization. Soc. Cogn. Affect. Neurosci. 12, 1–23 (2017).

    PubMed  Google Scholar 

  131. Finlay, B. & Uchiyama, R. Evolution of Nervous Systems (Oxford Academic Press, Oxford, 2017).

  132. Hauser, M. D., Chomsky, N. & Fitch, W. T. The faculty of language: what is it, who has it, and how did it evolve? Science 298, 1569–1579 (2002).

    Article  CAS  PubMed  Google Scholar 

  133. Bloom, P. Precis of How children learn the meanings of words. Behav. Brain Sci. 24, 1095–1103; discussion 1104–1034 (2001).

    Article  CAS  Google Scholar 

  134. Lupfer, G., Frieman, J. & Coonfield, D. Social transmission of flavor preferences in two species of hamsters (Mesocricetus auratus and Phodopus campbelli). J. Comp. Psychol. 117, 449–455 (2003).

    Article  PubMed  Google Scholar 

  135. Galef, B. G. & Laland, K. N. Social learning in animals: empirical studies and theoretical models. AIBS Bull. 55, 489–499 (2005).

    Google Scholar 

  136. Uller, T. Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23, 432–438 (2008).

    Article  PubMed  Google Scholar 

  137. Wolf, J. B. & Brodie, E. D. The coadaptation of parental and offspring characters. Evolution 52, 299–308 (1998).

    Article  PubMed  Google Scholar 

  138. Stigler, J. W., Shweder, R. A. & Herdt, G. (eds) Cultural Psychology 1–44 (Cambridge Univ. Press, New York, NY, 1990).

  139. Atzil, S. & Gendron, M. Bio-behavioral synchrony promotes the development of conceptualized emotions. Curr. Opin. Psychol. 17, 162–169 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  140. Gendron, M., Roberson, D. & Barrett, L. F. Cultural variation in emotion perception is real: a response to Sauter, Eisner, Ekman, and Scott (2015). Psychol. Sci. 26, 357–359 (2015).

    Article  PubMed  Google Scholar 

  141. Russell, J. A. Culture and the categorization of emotions. Psychol. Bull. 110, 426–450 (1991).

    Article  CAS  PubMed  Google Scholar 

  142. Andrews-Hanna, J. R. The brain’s default network and its adaptive role in internal mentation. Neuroscientist 18, 251–270 (2012).

    Article  PubMed  Google Scholar 

  143. Lombardo, M. V. et al. Shared neural circuits for mentalizing about the self and others. J. Cogn. Neurosci. 22, 1623–1635 (2010).

    Article  PubMed  Google Scholar 

  144. Gao, W. et al. Functional network development during the first year: relative sequence and socioeconomic correlations. Cereb. Cortex 25, 2919–2928 (2015).

    Article  PubMed  Google Scholar 

  145. Gao, W. et al. Evidence on the emergence of the brain’s default network from 2-week-old to 2-year-old healthy pediatric subjects. Proc. Natl Acad. Sci. USA 106, 6790–6795 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Supekar, K. et al. Development of functional and structural connectivity within the default mode network in young children. Neuroimage 52, 290–301 (2010).

    Article  PubMed  Google Scholar 

  147. Blakemore, S. J., den Ouden, H., Choudhury, S. & Frith, C. Adolescent development of the neural circuitry for thinking about intentions. Soc. Cogn. Affect. Neurosci. 2, 130–139 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  148. Alcauter, S. et al. Frequency of spontaneous BOLD signal shifts during infancy and correlates with cognitive performance. Dev. Cogn. Neurosci. 12, 40–50 (2015).

    Article  PubMed  Google Scholar 

  149. Uddin, L. Q., Supekar, K. S., Ryali, S. & Menon, V. Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. J. Neurosci. 31, 18578–18589 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Wegner, D. M. in Theories of Group Behavior (eds Mullen, B. & Goethals, G. R.) 185–208 (Springer, New York, NY, 1987).

  151. Syal, S. & Finlay, B. L. Thinking outside the cortex: social motivation in the evolution and development of language. Dev. Sci. 14, 417–430 (2011).

    Article  PubMed  Google Scholar 

  152. Dunbar, R. I. M. The social brain hypothesis. Evol. Anthropol. 6, 178–190 (1998).

    Article  Google Scholar 

  153. Gunnar, M. R. & Sullivan, R. M. The neurodevelopment of social buffering and fear learning: integration and crosstalk. Soc. Neurosci. 12, 1–7 (2017).

    Article  PubMed  Google Scholar 

  154. Coan, J. A., Schaefer, H. S. & Davidson, R. J. Lending a hand: social regulation of the neural response to threat. Psychol. Sci. 17, 1032–1039 (2006).

    Article  PubMed  Google Scholar 

  155. Master, S. L. et al. A picture’s worth: partner photographs reduce experimentally induced pain. Psychol. Sci. 20, 1316–1318 (2009).

    Article  PubMed  Google Scholar 

  156. Lantolf, J. P., Thorne, S. L. & Poehner, M. E. in Theories in Second Language Acquisition: An Introduction (eds VanPatten, B. & William, J.) 207–226 (Erlbaum, Mahwah, NJ, 2015).

  157. Padilla, A. M. & Perez, W. Acculturation, social identity, and social cognition: a new perspective. Hisp. J. Behav. Sci. 25, 35–55 (2003).

    Article  Google Scholar 

  158. Adolphs, R. The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60, 693–716 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  159. Frith, C. D. The social brain? Philos. Trans. R. Soc. London Ser. B 362, 671–678 (2007).

    Article  Google Scholar 

  160. Whitacre, J. M., Rohlfshagen, P., Bender, A. & Yao, X. Evolutionary mechanics: new engineering principles for the emergence of flexibility in a dynamic and uncertain world. Nat. Comput. 11, 431–448 (2012).

    Article  PubMed  Google Scholar 

  161. Boyd, R., Richerson, P. J. & Henrich, J. The cultural niche: why social learning is essential for human adaptation. Proc. Natl Acad. Sci. USA 108, 10918–10925 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Heyes, C. & Pearce, J. M. Not-so-social learning strategies. Proc. R. Soc. B 282, 1709–1715 (2015).

    Article  Google Scholar 

  163. Champagne, F. A. & Meaney, M. J. Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav. Neurosci. 121, 1353–1363 (2007).

    Article  PubMed  Google Scholar 

  164. Francis, D., Diorio, J., Liu, D. & Meaney, M. J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155–1158 (1999).

    Article  CAS  PubMed  Google Scholar 

  165. Lorenz, K. Der Kumpan in der Umwelt des Vogels. J. Ornithol. 83, 289–413 (1935).

    Article  Google Scholar 

  166. Lorenz, K. in Leaders in the Study of Animal Behavior: Autobiographical Perspectives (ed. Baerends, G. P.) 259–287 (Bucknell Univ. Press, Lewisburg, PA, 1985).

  167. Morton, J. & Johnson, M. H. CONSPEC and CONLERN: a two-process theory of infant face recognition. Psychol. Rev. 98, 164–181 (1991).

    Article  CAS  PubMed  Google Scholar 

  168. Braddick, O. Human development: faces in the womb. Curr. Biol. 27, R704–R706 (2017).

    Article  CAS  PubMed  Google Scholar 

  169. Cook, R., Bird, G., Catmur, C., Press, C. & Heyes, C. Mirror neurons: from origin to function. Behav. Brain Sci. 37, 177–192 (2014).

    Article  PubMed  Google Scholar 

  170. Turati, C., Di Giorgio, E., Bardi, L. & Simion, F. Holistic face processing in newborns, 3-month-old infants, and adults: evidence from the composite face effect. Child Dev. 81, 1894–1905 (2010).

    Article  PubMed  Google Scholar 

  171. Gava, L., Valenza, E., Turati, C. & de Schonen, S. Effect of partial occlusion on newborns’ face preference and recognition. Dev. Sci. 11, 563–574 (2008).

    Article  PubMed  Google Scholar 

  172. Turati, C., Bulf, H. & Simion, F. Newborns’ face recognition over changes in viewpoint. Cognition 106, 1300–1321 (2008).

    Article  PubMed  Google Scholar 

  173. Cassia, V. M., Turati, C. & Simion, F. Can a nonspecific bias toward top-heavy patterns explain newborns’ face preference? Psychol. Sci. 15, 379–383 (2004).

    Article  PubMed  Google Scholar 

  174. Simion, F., Leo, I., Turati, C., Valenza, E. & Dalla Barba, B. How face specialization emerges in the first months of life. Prog. Brain Res. 164, 169–185 (2007).

    Article  PubMed  Google Scholar 

  175. Turati, C. Why faces are not special to newborns: an alternative account of the face preference. Curr. Dir. Psychol. Sci. 13, 5–8 (2004).

    Article  Google Scholar 

  176. Gartstein, M. A. & Rothbart, M. K. Studying infant temperament via the revised infant behavior questionnaire. Infant Behav. Dev. 26, 64–86 (2003).

    Article  Google Scholar 

  177. Huffman, L. C. et al. Infant temperament and cardiac vagal tone: assessments at twelve weeks of age. Child Dev. 69, 624–635 (1998).

    Article  CAS  PubMed  Google Scholar 

  178. Davidov, M., Knafo-Noam, A., Serbin, L. A. & Moss, E. The influential child: how children affect their environment and influence their own risk and resilience. Dev. Psychopathol. 27, 947–951 (2015).

    Article  PubMed  Google Scholar 

  179. Rothbart, M. K. & Ahadi, S. A. Temperament and the development of personality. J. Abnorm. Psychol. 103, 55 (1994).

    Article  CAS  PubMed  Google Scholar 

  180. George, O., Le Moal, M. & Koob, G. F. Allostasis and addiction: role of the dopamine and corticotropin-releasing factor systems. Physiol. Behav. 106, 58–64 (2012).

    Article  CAS  PubMed  Google Scholar 

  181. Koob, G. F. & Le Moal, M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24, 97–129 (2001).

    Article  CAS  PubMed  Google Scholar 

  182. Beauchaine, T. P., Neuhaus, E., Zalewski, M., Crowell, S. E. & Potapova, N. The effects of allostatic load on neural systems subserving motivation, mood regulation, and social affiliation. Dev. Psychopathol. 23, 975–999 (2011).

    Article  PubMed  Google Scholar 

  183. Buckner, R. L., Andrews-Hanna, J. R. & Schacter, D. L. The brain’s default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1–38 (2008).

    Article  PubMed  Google Scholar 

  184. Young, L. J. & Barrett, C. E. Neuroscience. Can oxytocin treat autism? Science 347, 825–826 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Farmer, C., Thurm, A. & Grant, P. Pharmacotherapy for the core symptoms in autistic disorder: current status of the research. Drugs 73, 303–314 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Pellicano, E. & Burr, D. When the world becomes ‘too real’: a Bayesian explanation of autistic perception. Trends Cogn. Sci. 16, 504–510 (2012).

    Article  PubMed  Google Scholar 

  187. Verly, M. et al. Altered functional connectivity of the language network in ASD: role of classical language areas and cerebellum. Neuroimage Clin. 4, 374–382 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  188. Jaffe-Dax, S., Frenkel, O. & Ahissar, M. Dyslexics’ faster decay of implicit memory for sounds and words is manifested in their shorter neural adaptation. Elife 6, e20557 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  189. Jaffe-Dax, S., Raviv, O., Jacoby, N., Loewenstein, Y. & Ahissar, M. Towards a computational model of Dyslexia. BMC Neurosci. 16, O12 (2015).

    Article  PubMed Central  Google Scholar 

  190. Leerkes, E. M., Su, J., Calkins, S. D., O’Brien, M. & Supple, A. J. Maternal physiological dysregulation while parenting poses risk for infant attachment disorganization and behavior problems. Dev. Psychopathol. 29, 1–13 (2016).

    Google Scholar 

  191. Tasker, F. Lesbian mothers, gay fathers, and their children: a review. J. Dev. Behav. Pediatr. 26, 224–240 (2005).

    Article  PubMed  Google Scholar 

  192. Bornstein, M. H. & Bradley, R. H. Socioeconomic Status, Parenting, and Child Development (Routledge, New York, NY, 2014).

  193. Merz, E. C., Tottenham, N. & Noble, K. G. Socioeconomic status, amygdala volume, and internalizing symptoms in children and adolescents. J. Clin. Child Adolesc. Psychol. 47, 312–323 (2018).

    Article  PubMed  Google Scholar 

  194. Kolb, B., Gibb, R. & Robinson, T. E. Brain plasticity and behavior. Curr. Dir. Psychol. Sci. 12, 1–5 (2003).

    Article  Google Scholar 

  195. Metcalfe, N. B., Taylor, A. C. & Thorpe, J. E. Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim. Behav. 49, 431–436 (1995).

    Article  Google Scholar 

  196. Leonard, W. R. & Robertson, M. L. Evolutionary perspectives on human nutrition: the influence of brain and body size on diet and metabolism. Am. J. Hum. Biol. 6, 77–88 (1994).

    Article  PubMed  Google Scholar 

  197. Dunbar, R. I. The social brain hypothesis and its implications for social evolution. Ann. Hum. Biol. 36, 562–572 (2009).

    Article  CAS  PubMed  Google Scholar 

  198. Soares, C. A. & Carneiro, R. S. Social behavior between mothers’ young of sloths Bradypus variegatus Schinz, 1825 (Xenarthra: Bradypodidae). Braz. J. Biol. 62, 249–252 (2002).

    Article  CAS  PubMed  Google Scholar 

  199. Richard, A. F. & Nicoll, M. E. Female social dominance and basal metabolism in a Malagasy primate. Propithecus verreauxi. Am. J. Primatol. 12, 309–314 (1987).

    Article  PubMed  Google Scholar 

  200. Curley, J. P. & Keverne, E. B. Genes, brains and mammalian social bonds. Trends Ecol. Evol. 20, 561–567 (2005).

    Article  PubMed  Google Scholar 

  201. Schulkin, J. Allostasis, Homeostasis, and the Costs of Physiological Adaptation (Cambridge Univ. Press, Cambridge, 2004).

  202. Shpigler, H. Y. et al. Deep evolutionary conservation of autism-related genes. Proc. Natl Acad. Sci. USA 36, 9653–9658 (2017).

    Article  CAS  Google Scholar 

  203. Gao, W., Alcauter, S., Smith, J. K., Gilmore, J. H. & Lin, W. Development of human brain cortical network architecture during infancy. Brain Struct. Funct. 220, 1173–1186 (2015).

    Article  PubMed  Google Scholar 

  204. Sepulcre, J., Sabuncu, M. R., Yeo, T. B., Liu, H. & Johnson, K. A. Stepwise connectivity of the modal cortex reveals the multimodal organization of the human brain. J. Neurosci. 32, 10649–10661 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Xu, P. et al. Different topological organization of human brain functional networks with eyes open versus eyes closed. Neuroimage 90, 246–255 (2014).

    Article  PubMed  Google Scholar 

  206. Sterzer, P. & Kleinschmidt, A. Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct. Funct. 214, 611–622 (2010).

    Article  PubMed  Google Scholar 

  207. Angelaki, D. E., Gu, Y. & DeAngelis, G. C. Multisensory integration: psychophysics, neurophysiology, and computation. Curr. Opin. Neurobiol. 19, 452–458 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank K. Toledano for his contribution to the illustrations.

Author information

Authors and Affiliations

Authors

Contributions

S.A., W.G. I.F. and L.F.B. contributed to writing the manuscript.

Corresponding authors

Correspondence to Shir Atzil or Lisa Feldman Barrett.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Table 1

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Atzil, S., Gao, W., Fradkin, I. et al. Growing a social brain. Nat Hum Behav 2, 624–636 (2018). https://doi.org/10.1038/s41562-018-0384-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41562-018-0384-6

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing