Reward sensitivity for a palatable food reward peaks during pubertal developmental in rats

Abstract

Puberty is a critical period for the initiation of drug use and abuse. Because early drug use onset often accounts for a more severe progression of addiction, it is of importance to understand the underlying mechanisms and neurodevelopmental changes during puberty that are contributing to enhanced reward processing in teenagers. The present study investigated the progression of reward sensitivity toward a natural food reward over the whole course of adolescence in male rats (postnatal days 30-90) by monitoring consummatory, motivational behavior and neurobiological correlates of reward. Using a limited-free intake paradigm, consumption of sweetened condensed milk (SCM) was measured repeatedly in adolescent and adult rats. Additionally, early- and mid-pubertal animals were tested in Progressive Ratio responding for SCM and c-fos protein expression in reward-associated brain structures was examined after odor conditioning for SCM. We found a transient increase in SCM consumption and motivational incentive for SCM during puberty. This increased reward sensitivity was most pronounced around mid-puberty. The behavioral findings are paralleled by enhanced c-fos staining in reward-related structures revealing an intensified neuronal response after reward-cue presentation, distinctive for pubertal animals. Taken together, these data indicate an increase in reward sensitivity during adolescence accompanied by enhanced responsiveness of reward-associated brain structures to incentive stimuli, and it seems that both is strongly pronounced around mid-puberty. Therefore, higher reward sensitivity during pubertal maturation might contribute to the enhanced vulnerability of teenagers for the initiation of experimental drug use.

Keywords: c-fos; food reward; motivation; puberty; reward sensitivity.

Figure 1

Mean SCM intake relative to body weight in adolescent rats between age pd 30 and pd 90 (A) and in adult rats (starting at pd 100) (B). SCM intake was increased during early and mid-adolescence (pd 30–60) compared to young adulthood (pd 70–90). A peak was observed on pd 50 that differed significantly from all other testing days. No statistical differences were observed after repeated testing in adult rats (B). In addition, the average SCM consumption of pubertal rats (PND 40–60) differed significantly from adult animals on pd 90 (C). Asterisks (*) and (**) indicate significant differences at p-levels of p ≤ 0.05 and p ≤ 0.01, respectively. Data are expressed as mean ± SEM.

Figure 2

Mean body weight and percentage weight gain during adolescence. Points indicate mean body weight of rats between an age of PND 30 to PND 90 (left scale). Bars indicate the percentaged weight gain in relation to previous body weight (right scale). The highest weight gain was observed during pubertal development, with a peak just shortly before puberty onset from pd 30 to 40. Asterisks (*) indicate significant differences at p-levels of p ≤ 0.05. Data are expressed as mean ± SEM.

Figure 3

Progressive Ratio performance of early- (pd 40), mid-pubertal (pd 50) and adult rats (pd 90). The figure depicts total lever presses (A), HCR (B) and the break point (IR) (C). Performance of mid-pubertal rats differed significantly from early-pubertal and adult animals for total lever presses and HCR. Asterisks (*) and (**) indicate significant differences at p-levels of p ≤ 0.05 and p ≤ 0.01, respectively. Data are expressed as mean ± SEM.

Figure 4

c-fos protein expression after presentation of the SCM odor cue. Mean c-fos positive cell counts in NACc (A), NACs (B) and dStr (C) of early- (pd 40), mid-pubertal (pd 50) and adult rats (pd 90) that were either sham-trained or trained for odor-reward association. No statistical differences in c-fos expression were observed between sham-trained groups. However, in trained rats both pubertal groups expressed significantly more c-fos activated cells in comparison to adult rats in NACc and dStr. Asterisks (*) indicate significant differences at p-levels of p ≤ 0.05. Data are expressed as mean ± SEM.

Figure 5

Schematic diagram of a coronal section of a rat brain adopted from Paxinos and Watson (1998) rat brain atlas at sampling section level of +1.7 mm from bregma. Within each region of interest a 250 μm × 250 μm was randomly placed for cell counting. Pictures show c-fos staining with DAB in dStr (top) and NACc (bottom) at 20× magnification for rats undergoing either odor conditioning (trained) or sham training (sham).