Pubertal Development, but not Hormone Levels, is Associated with Reduced Response to Reward

• In Event: Embracing the Complexities of Adolescence: The Role of Pubertal Maturation and Hormones on Neurodevelopment

Abstract

Introduction: Reward processing is key for a variety of human activities (Banji & Delgado, 2013) and is important to study because it is linked to maladaptive behaviors (Braams, et al., 2016). Neurally, ventral striatum is critical for reward processing (Schultz, et al., 1997). Adolescents are more reward sensitive than children or adults (Casey, et al., 2019), with increased reward activation across adolescence peaking at about age 15 (Braams, et al., 2015). There is some evidence that increases in reward responsiveness are associated with increases in pubertal hormones (Braams, et al., 2015). However, this is not always observed (e.g., Ladouceur, et al., 2019). Here, early and mid-adolescents were longitudinally examined using a reward processing task during fMRI where the role of hormones and physical development in modulating response to reward was explored. Methods: A total of 124 youth participated in a longitudinal study. Females were 10-12 years and males were 11- 13 years to be roughly equivalent in terms of pubertal development. At wave 1, 66 youth provided usable fMRI data and 118 youth provided usable hormone data. Two years later, at wave 2, 42 youth provided usable fMRI data and 79 youth provided usable hormone data. Attrition in MRI data was largely due to contraindications to scanning and excessive movement. During fMRI, youth identified a gopher amongst 4 target animals. In 31 out of 61 trials, correct responses engendered reward; in 30 trials, correct responses remained unrewarded. Basal testosterone and DHEA were assayed at each wave from three waking saliva samples provided over 1 month. Tanner staging was completed by a medical researcher to assess pubertal development as well as youth self-report. Regions of interest in left ventral striatum, right ventral striatum, and vmPFC were created from a reward processing meta-analysis (Clithero & Rangel, 2014). The differences in average activations to rewarded and non-rewarded trials from each region were modeled as outcome variables. Data was analyzed using Hierarchical Linear Modeling to account for longitudinal changes in developmental processes. Results: Less difference between striatum activation to rewarded and non-rewarded trials was observed at wave 2 relative to wave 1. Adrenally-driven pubertal development was associated with reduced difference in activation to rewarded and non-rewarded trials at wave 2 relative to wave 1 in left [= -.067, p=.006] and right ventral striatum [= -.028, p=.011]. A similar find was observed for gonadally-driven pubertal development in right ventral striatum [= -.027, p=.008], but not left ventral striatum [= -.008, p=.488]. Testosterone and DHEA were not significantly associated with differences in activation to rewarded and non-rewarded trials at wave 2 relative to wave 1 [ps>.187]. Discussion: These data suggest that physical markers of pubertal development are associated with reduced sensitivity to reward more so than variation in hormonal levels. The relative contributions of physical development related to puberty versus pubertal hormones in altering behaviors in adolescence remains unclear. The current data suggest that physical development may be more influential in altering reward responsiveness.

Authors

• Stuart White, Boys Town National Research Hospital
  Presenting Author

• Elizabeth A. Shirtcliff, Iowa State University
  Non-Presenting Author

• Yoojin Lee
  Non-Presenting Author

• Jenny Mai Phan, University of Wisconsin-Madison
  Non-Presenting Author

• Cecile D Ladouceur, University of Pittsburgh
  Non-Presenting Author