A Rapid Peak in Gamma Power Signals Critical Period Plasticity in the Developing Mouse Visual Cortex

Abstract

Experience sculpts neural circuits during discrete windows of postnatal development termed critical periods. This process allows the brain to adapt to its environment and efficiently allocate resources. However, maladaptive experience can also be consolidated early in life, reducing the effectiveness of interventions in adulthood. Critical periods across the cortex open and close at different times during postnatal development; the timing of these windows is set by the balance of excitation and inhibition. Cortical rhythms, particularly in the gamma power band (30-80 Hz), are sensitive to shifts in this balance. However, initial changes in oscillatory activity following sensory deprivation remain unknown. Rhythmic activity is disrupted in many neurological disorders, including autism and schizophrenia; a deeper understanding of the role oscillations play in developing circuits will inform disease treatment. In this work we use EEG recording in mice to assess changes in cortical oscillations during a classic critical period paradigm, ocular dominance plasticity. Deprivation of visual input induces a rapid rise in rhythmic activity at 40 Hz over the visual cortex which persists for up to two hours. This increase in gamma power only occurs when mice are in the critical period for ocular dominance plasticity; adult mice do not show a change, suggesting that the rise in gamma may signal a plastic cortical state. To confirm this, we correlated the rise in gamma with plasticity in several mouse models with shifted critical periods. Finally, selectively manipulating rhythmic activity in adult mice was able to restore cortical plasticity, suggesting that the rise in gamma power is playing an active role in the plasticity process. Taken together, our data reveal EEG gamma power to be a robust indicator of the early stages of critical period plasticity, and may serve as a useful biomarker to assess the plastic capacity in human cortex. In addition, direct modulation of gamma power using techniques such as transcranial magnetic stimulation or learned entrainment may have therapeutic benefit for the restoration of function in adults.