Early childhood stress exposure, reward pathways, and adult decision making
Rasmus M Birn, Barbara J Roeber, Seth D Pollak, Rasmus M Birn, Barbara J Roeber, Seth D Pollak
Abstract
Individuals who have experienced chronic and high levels of stress during their childhoods are at increased risk for a wide range of behavioral problems, yet the neurobiological mechanisms underlying this association are poorly understood. We measured the life circumstances of a community sample of school-aged children and then followed these children for a decade. Those from the highest and lowest quintiles of childhood stress exposure were invited to return to our laboratory as young adults, at which time we reassessed their life circumstances, acquired fMRI data during a reward-processing task, and tested their judgment and decision making. Individuals who experienced high levels of early life stress showed lower levels of brain activation when processing cues signaling potential loss and increased responsivity when actually experiencing losses. Specifically, those with high childhood stress had reduced activation in the posterior cingulate/precuneus, middle temporal gyrus, and superior occipital cortex during the anticipation of potential rewards; reduced activation in putamen and insula during the anticipation of potential losses; and increased left inferior frontal gyrus activation when experiencing an actual loss. These patterns of brain activity were associated with both laboratory and real-world measures of individuals' risk taking in adulthood. Importantly, these effects were predicated only by childhood stress exposure and not by current levels of life stress.
Keywords: childhood development; decision making; early life stress; reward; social behavior.
Conflict of interest statement
The authors declare no conflict of interest.
Copyright © 2017 the Author(s). Published by PNAS.
Figures
References
- Shonkoff JP, Garner AS. Committee on Psychosocial Aspects of Child and Family Health Committee on Early Childhood, Adoption, and Dependent Care Section on Developmental and Behavioral Pediatrics The lifelong effects of early childhood adversity and toxic stress. Pediatrics. 2012;129:e232–e246.
- Norman RE, et al. The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. PLoS Med. 2012;9:e1001349.
- Pechtel P, Pizzagalli DA. Effects of early life stress on cognitive and affective function: An integrated review of human literature. Psychopharmacology (Berl) 2011;214:55–70.
- Evans GW, Li D, Whipple SS. Cumulative risk and child development. Psychol Bull. 2013;139:1342–1396.
- Cabib S, Puglisi-Allegra S. Stress, depression and the mesolimbic dopamine system. Psychopharmacology (Berl) 1996;128:331–342.
- Hollon NG, Burgeno LM, Phillips PE. Stress effects on the neural substrates of motivated behavior. Nat Neurosci. 2015;18:1405–1412.
- Matthews K, Robbins TW. Early experience as a determinant of adult behavioural responses to reward: The effects of repeated maternal separation in the rat. Neurosci Biobehav Rev. 2003;27:45–55.
- Knutson B, Fong GW, Adams CM, Varner JL, Hommer D. Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport. 2001;12:3683–3687.
- Knutson B, Westdorp A, Kaiser E, Hommer D. FMRI visualization of brain activity during a monetary incentive delay task. Neuroimage. 2000;12:20–27.
- Knutson B, Adams CM, Fong GW, Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci. 2001;21:RC159.
- Pryce CR, Dettling AC, Spengler M, Schnell CR, Feldon J. Deprivation of parenting disrupts development of homeostatic and reward systems in marmoset monkey offspring. Biol Psychiatry. 2004;56:72–79.
- Berridge KC, Robinson TE. Liking, wanting, and the incentive-sensitization theory of addiction. Am Psychol. 2016;71:670–679.
- Boecker R, et al. Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years. PLoS One. 2014;9:e104185.
- Balodis IM, et al. Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biol Psychiatry. 2012;71:749–757.
- Choi JS, et al. Altered brain activity during reward anticipation in pathological gambling and obsessive-compulsive disorder. PLoS One. 2012;7:e45938.
- Harms MB, Shannon Bowen KE, Hanson JL, Pollak SD. Instrumental learning and cognitive flexibility processes are impaired in children exposed to early life stress. Dev Sci. October 19, 2017 doi: 10.1111/desc.12596.
- Dillon DG, et al. Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biol Psychiatry. 2009;66:206–213.
- Enzi B, et al. Alterations of monetary reward and punishment processing in chronic cannabis users: An fMRI study. PLoS One. 2015;10:e0119150.
- Chua HF, Gonzalez R, Taylor SF, Welsh RC, Liberzon I. Decision-related loss: Regret and disappointment. Neuroimage. 2009;47:2031–2040.
- Knutson B, Greer SM. Anticipatory affect: Neural correlates and consequences for choice. Philos Trans R Soc Lond B Biol Sci. 2008;363:3771–3786.
- Kanwisher N, Wojciulik E. Visual attention: Insights from brain imaging. Nat Rev Neurosci. 2000;1:91–100.
- Cavanna AE, Trimble MR. The precuneus: A review of its functional anatomy and behavioural correlates. Brain. 2006;129:564–583.
- Pollak SD. Multilevel developmental approaches to understanding the effects of child maltreatment: Recent advances and future challenges. Dev Psychopathol. 2015;27:1387–1397.
- Kumar P, et al. Differential effects of acute stress on anticipatory and consummatory phases of reward processing. Neurosci. 2014;266:1–12.
- Lemos JC, et al. Severe stress switches CRF action in the nucleus accumbens from appetitive to aversive. Nature. 2012;490:402–406.
- Hammen C, et al. Children of depressed mothers: Maternal strain and symptom predictors of dysfunction. J Abnorm Psychol. 1987;96:190–198.
- Eaton DK, et al. Centers for Disease Control and Prevention (CDC) Youth risk behavior surveillance United States, 2011. MMWR Surveill Summ. 2012;61:1–162.
- Cox RW. AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 1996;29:162–173.
- Cox RW, Chen G, Glen DR, Reynolds RC, Taylor PA. fMRI clustering and false-positive rates. Proc Natl Acad Sci USA. 2017;114:E3370–E3371.
- Cox RW, Chen G, Glen DR, Reynolds RC, Taylor PA. fMRI clustering in AFNI: False-positive rates redux. Brain Connect. 2017;7:152–171.
- MacKinnon DP, Lockwood CM, Hoffman JM, West SG, Sheets V. A comparison of methods to test mediation and other intervening variable effects. Psychol Methods. 2002;7:83–104.
Source: PubMed