Sensory experience is widely thought to drive activity levels in the cortex. In adult animals, chronic modifications of sensory activity, such as visual deprivation, lead to compensatory changes in synaptic strength. The postsynaptic mechanisms that underpin modifications of synaptic strength have been studied in great detail. In contrast, the presynaptic mechanisms that are altered following a change in cortical activity are less well understood. Here we study presynaptic axonal boutons of excitatory axons in superficial layers of the adult mouse primary visual cortex following enucleation. We found greater bouton turnover at excitatory axons in the cortex of mice with reduced visually driven activity (deprived). Persistent boutons fluctuated in a size dependent manner; so that large boutons became smaller whilst smaller boutons became bigger. This shift in the synaptic ‘weighting’ of individual boutons was balanced so that the population average remained constant. Functional analysis of the paired pulse ratio was consistent with a remapping of synaptic weights so that synaptic dynamics shifted from largely depression to a combination of weak depression and facilitation. One mechanism that might account for regulation of this process is the sharing of a finite pool of local presynaptic machinery. We propose that this is a form of presynaptic homeostasis.