Strong gamma frequency oscillations in the adolescent prefrontal cortex

Abstract

Working memory ability continues to mature into adulthood in both humans and non-human 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 (LFP) provide a window into the computation carried out 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 stage. Simultaneous single-unit and LFP signals were recorded from areas 8a and 46 of the dorsolateral prefrontal cortex (dlPFC). In both the cue and delay period, power relative to baseline increased in the gamma frequency range (32 - 128 Hz). 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. Gamma power and neuronal firing did not show stronger temporal correlations. Our results establish gamma power decrease to be a feature of prefrontal cortical maturation. Significance StatementGamma-frequency oscillations in extracellular field recordings (such as LFP 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 non-human 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 and raise the possibility that schizophrenia represent an excessive state of prefrontal maturation.