Abstract
Mature behaviors emerge from neural circuits sculpted by genetic programs and spontaneous and evoked neural activity. However, how neural activity is refined to drive maturation of learned behavior remains poorly understood. Here, we explore how transient hormonal signaling coordinates a neural activity state transition and maturation of associative learning. We identify spontaneous, asynchronous activity in a Drosophila learning and memory brain region, the mushroom body. This activity declines significantly over the first week of adulthood. Moreover, this activity is generated cell-autonomously via Cacophony voltage-gated calcium channels in a single cell type, α'/β' Kenyon cells. Juvenile hormone, a crucial developmental regulator, acts transiently in α'/β' Kenyon cells during a young adult sensitive period to downregulate spontaneous activity and enable subsequent enhanced learning. Hormone signaling in young animals therefore controls a neural activity state transition and is required for improved associative learning, providing insight into the maturation of circuits and behavior.
Highlights
Genetic programs and experience in the form of neural activity refine neural circuits, sculpting cognitive function over time
Temporal evolution of spontaneous neural activity patterns is prevalent in developing circuits, the molecular mechanisms that control the timing of neural activity state transitions and coordinate maturation of behavioral outputs in young animals are largely unknown
Asynchronous activity in one mushroom body (MB) cell type, the a0/b0 Kenyon cells (KCs), in young animals, which unexpectedly declines over the first week of adulthood
Summary
Genetic programs and experience in the form of neural activity refine neural circuits, sculpting cognitive function over time. Activity state transitions in neural circuits are widespread during normal development (Akin et al, 2019; Ben-Ari et al, 1989; Blankenship and Feller, 2010; Farooq and Dragoi, 2019; Piekarski et al, 2017). Periodic waves of spontaneous neural activity occur throughout immature visual, somatosensory, and motor brain regions in perinatal critical periods, before distinct, less correlated sensory-evoked or locomotion-related activity patterns emerge in older animals (Blankenship and Feller, 2010). Temporal evolution of spontaneous neural activity patterns is prevalent in developing circuits, the molecular mechanisms that control the timing of neural activity state transitions and coordinate maturation of behavioral outputs in young animals are largely unknown
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