Experience leaves a lasting structural trace in cortical circuits

Abstract

It is common knowledge that early experience improves the brain's ability to adapt to similar events in the future, but it is not clear how the original experience is represented in neuronal circuits, or how it contributes to re-learning. The model of the temporary closure of one eye in mice provides a system in which such questions can be tackled. The new experience — monocular vision — induces growth of dendritic spines from nerve cells in the visual cortex. By alternating periods of monocular and binocular vision and following the morphology of the nerve cells for several days, Hofer et al. were able to record the experience-induced structural changes and to discover if they outlast the experience itself. They find that long-lived dendritic spine density increases in response to monocular deprivation and persists beyond the duration of the experience. Subsequent deprivation fails to induce further spine density increases, suggesting initial experience may provide a structural experience 'trace' that can be utilized in response to further functional shifts. Dendritic spine morphogenesis is sensitive to experience-dependent plasticity, but whether or not experience-induced structural changes outlast the experience itself is unknown. This paper reveals that long-lived spine density increases in response to monocular deprivation that persist beyond the duration of time the eye was closed. Subsequent deprivation fails to induce further spine density increases, suggesting initial experience may provide a structural experience 'trace' that could be utilized in response to further functional shifts. Sensory experiences exert a powerful influence on the function and future performance of neuronal circuits in the mammalian neocortex1,2,3. Restructuring of synaptic connections is believed to be one mechanism by which cortical circuits store information about the sensory world4,5. Excitatory synaptic structures, such as dendritic spines, are dynamic entities6,7,8 that remain sensitive to alteration of sensory input throughout life6,9. It remains unclear, however, whether structural changes at the level of dendritic spines can outlast the original experience and thereby provide a morphological basis for long-term information storage. Here we follow spine dynamics on apical dendrites of pyramidal neurons in functionally defined regions of adult mouse visual cortex during plasticity of eye-specific responses induced by repeated closure of one eye (monocular deprivation). The first monocular deprivation episode doubled the rate of spine formation, thereby increasing spine density. This effect was specific to layer-5 cells located in binocular cortex, where most neurons increase their responsiveness to the non-deprived eye3,10. Restoring binocular vision returned spine dynamics to baseline levels, but absolute spine density remained elevated and many monocular deprivation-induced spines persisted during this period of functional recovery. However, spine addition did not increase again when the same eye was closed for a second time. This absence of structural plasticity stands out against the robust changes of eye-specific responses that occur even faster after repeated deprivation3. Thus, spines added during the first monocular deprivation experience may provide a structural basis for subsequent functional shifts. These results provide a strong link between functional plasticity and specific synaptic rearrangements, revealing a mechanism of how prior experiences could be stored in cortical circuits.