Experience-dependent structural plasticity in the adult brain: How the learning brain grows

•Perception learning causes a transient increase in brain grey matter volume detectable by MRI.•This learning results in pronounced changes of neuronal dendrites and an increase in the number of dendritic spines.•Structural neuronal plasticity is associated with a reorganization and transient swelling of astrocytes.•Brain volume and astrocyte volume return to baseline post-learning, with a persistent increase in the number of mature spines. Volumetric magnetic resonance imaging studies have shown that intense learning can be associated with grey matter volume increases in the adult brain. The underlying mechanisms are poorly understood. Here we used monocular deprivation in rats to analyze the mechanisms underlying use-dependent grey matter increases. Optometry for quantification of visual acuity was combined with volumetric magnetic resonance imaging and microscopic techniques in longitudinal and cross-sectional studies. We found an increased spatial vision of the open eye which was associated with a transient increase in the volumes of the contralateral visual and lateral entorhinal cortex. In these brain areas dendrites of neurons elongated, and there was a strong increase in the number of spines, the targets of synapses, which was followed by spine maturation and partial pruning. Astrocytes displayed a transient pronounced swelling and underwent a reorganization of their processes. The use-dependent increase in grey matter corresponded predominantly to the swelling of the astrocytes. Experience-dependent increase in brain grey matter volume indicates a gain of structure plasticity with both synaptic and astrocyte remodeling.