Strong Gamma Frequency Oscillations in the Adolescent Prefrontal Cortex.

Abstract

Working memory ability continues to mature into adulthood in humans and nonhuman primates. At the single-neuron level, adolescent development is characterized by increased prefrontal firing rate in the delay period, but less is known about how coordinated activity between neurons is altered. Local field potentials (LFPs) provide a window into the computations conducted by the local network. To address the effects of adolescent development on LFP activity, three male rhesus monkeys were trained to perform an oculomotor delayed response task and tested at both the adolescent and adult stages. Simultaneous single-unit and LFP signals were recorded from areas 8a and 46 of the dorsolateral prefrontal cortex. In both the cue and delay period, power relative to baseline in the gamma frequency range (32-128 Hz) was higher in the adolescent than the adult stage. The changes between developmental stages could not be accounted for by differences in performance and were observed in more posterior as well as more anterior recording sites. In the adult stage, high-firing neurons were also more likely to reside at sites with strong gamma power increase from baseline. For both stages, the gamma power increase in the delay was selective for sites with neuron-encoding stimulus information in their spiking. Our results establish gamma power decrease to be a feature of prefrontal cortical maturation.SIGNIFICANCE STATEMENT Gamma-frequency oscillations in extracellular field recordings (e.g., local field potential or EEG) are a marker of normal interactions between excitatory and inhibitory neurons in neural circuits. Abnormally low gamma power during working memory is seen in conditions such as schizophrenia. We sought to examine whether the immature prefrontal cortex similarly exhibits lower power in the gamma-frequency range during working memory, in a nonhuman primate model of adolescence. Contrary to this expectation, the adolescent PFC exhibited stronger gamma power during the maintenance of working memory. Our findings reveal an unknown developmental maturation trajectory of gamma-band oscillations, propose a refinement of information encoding during PFC maturation, and raise the possibility that schizophrenia represents an excessive state of prefrontal maturation.