Reduced Neuronal Inhibition and Coordination of Adolescent Prefrontal Cortex during Motivated Behavior

Adolescent and adult OFC LFPs during sessions 3–6. A, LFP power spectra for adolescents and adults in windows around key task events were normalized to the baseline period (3 to 1 s before cue onset) for each frequency. The time course of normalized LFP power was primarily similar between adolescents and adults. At cue onset, both groups exhibited slight reductions in gamma (>30 Hz) power. This was also observed around the instrumental response. Adults and adolescents both exhibited slightly increased beta (13–30 Hz) power at this time. Immediately after reinforcement, adolescents and adults had increases in theta (4–7 Hz), alpha (8–12 Hz), beta, and gamma power, with adults showing greater increases in the alpha and beta bands. Adolescents had greater increases in high gamma power (above ∼75 Hz). B, Time course of adolescent and adult normalized LFP power around reinforcement. Line graphs correspond to baseline-normalized adolescent and adult LFP power averaged across discrete frequency bands as labeled.

Fano factor analysis comparing adolescent and adult firing-rate variability. The Fano factor is the slope of the trial-by-trial spike-count variance and spike-count mean for all units. Using a sliding window, this variability estimate was computed at time points around task events of interest. Fitted polynomial lines are plotted over raw Fano factor values. For both groups, the instrumental response and the period preceding entry into the food trough were accompanied by reductions in the Fano factor. Adolescents tended to have higher Fano factors than adults. Specifically, adolescents had greater Fano factors during the baseline period, in the 1 s after the trial-onset cue, in a 1 s window around the instrumental poke, and in the 1 s leading up to reinforcement retrieval. These results were not attributable to time- or age-dependent firing-rate differences, because this pattern survived a mean-matching procedure that controls for changes in firing rate (supplemental Fig. 3, available at www.jneurosci.org as supplemental material).

Average baseline-normalized firing rate + 1 SEM (shading) for all adult and adolescent units, time-locked to task events during each of six sessions. The median taskwide firing rate for all adolescent units was 4.66 Hz, and all adult units was 5.18 Hz. Although slight, their corresponding firing-rate distributions were significantly different (rank-sum test, Z = 2.18, p = 0.03). This figure demonstrates that, in session 1 (adult, n = 47; adolescent, n = 60; first row), when the action–outcome association was not yet learned (Fig. 1c), there was little task-related activity to the cue (left), instrumental pokes (middle), or rewarded food-trough entries (right) in either group. By session 2 (adult, n = 59; adolescent, n = 60; second row), as animals learned at different rates and performed the task to varying extents, average OFC neural activity began to change around task events in both groups. From session 3 onward (session 3: adult, n = 49; adolescent, n = 64; session 4: adult, n = 46; adolescent, n = 67; session 5: adult, n = 41; adolescent, n = 72; session 6: adult, n = 48; adolescent, n = 62; third to sixth rows), average normalized neural activity settled into somewhat stable patterns in both age groups.