Abstract
Gamma oscillations are a prominent activity pattern in the cerebral cortex. While gamma rhythms have been extensively studied in the adult prefrontal cortex in the context of cognitive (dys)functions, little is known about their development. We addressed this issue by using extracellular recordings and optogenetic stimulations in mice across postnatal development. We show that fast rhythmic activity in the prefrontal cortex becomes prominent during the second postnatal week. While initially at about 15 Hz, fast oscillatory activity progressively accelerates with age and stabilizes within gamma frequency range (30-80 Hz) during the fourth postnatal week. Activation of layer 2/3 pyramidal neurons drives fast oscillations throughout development, yet the acceleration of their frequency follows similar temporal dynamics as the maturation of fast-spiking interneurons. These findings uncover the development of prefrontal gamma activity and provide a framework to examine the origin of abnormal gamma activity in neurodevelopmental disorders.
Highlights
Synchronization of neuronal activity in fast oscillatory rhythms is a commonly observed feature in the adult cerebral cortex
Fast inhibitory feedback via soma-targeting parvalbumin (PV)-expressing inhibitory interneurons leads to fast gamma activity (30–80 Hz) (Cardin et al, 2009; Chen et al, 2017), whereas dendrite-targeting somatostatin (SOM)-expressing inhibitory interneurons contribute to beta/low gamma activity (20–40 Hz) (Chen et al, 2017; Veit et al, 2017)
Fast oscillatory activity in the prefrontal cortex accelerates during development Extracellular recordings in the medial prefrontal cortex (mPFC) of anesthetized and non-anesthetized P5-40 mice revealed that oscillatory activity at fast frequencies (>12 Hz) can be detected at the beginning of the second postnatal week
Summary
Synchronization of neuronal activity in fast oscillatory rhythms is a commonly observed feature in the adult cerebral cortex. While its exact functions are still a matter of debate, oscillatory activity in gamma frequency range has been proposed to organize neuronal ensembles and to shape information processing in cortical networks (Singer, 2018; Cardin, 2016; Sohal, 2016). Gamma activity emerges from reciprocal interactions between excitatory and inhibitory neurons. A fine-tuned balance between excitatory drive and inhibitory feedback is mandatory for circuit function underlying cognitive performance. Imbalance between excitation and inhibition in cortical networks and resulting gamma disruption have been proposed to cause cognitive disabilities in autism and schizophrenia (Cho et al, 2015; Cao et al, 2018; Rojas and Wilson, 2014)
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