Astrocytes are key supporters of brain functioning that are well documented to influence neural circuits over slow and prolonged timescales. Astrocytes in striatum regulate the extracellular neuromodulator landscape that governs dopamine transmission. We explored whether striatal astrocytes might act dynamically within striatal circuits to govern dopamine function. Surprisingly, we show that striatal astrocytes rapidly modulate dopamine release on a subsecond timescale. Brief optogenetic depolarisation of striatal astrocytes in mouse ex vivo brain slices strongly and reversibly modulated dopamine release as detected with fast-scan cyclic voltammetry, mediated via activation of nicotinic acetylcholine receptors on dopaminergic axons. We used immunocytochemical techniques to explore the anatomical localisation of mouse striatal astrocytes. We found astrocytes to be commonly apposed to the soma of cholinergic interneurons (ChIs) in a satellite configuration, a feature rarely observed for striatal projection neurons. Using patch-clamp recordings of ChIs and astrocytes, we reveal a rapid and strong reciprocal modulation of activity. This reciprocal interaction could have profound implications for the operation of striatal circuitry. We are additionally investigating functional and anatomical changes in striatal astrocytes in an alpha-synuclein-overexpressing mouse model of early Parkinson’s disease and human post mortem tissue. Together, these findings suggest a bidirectional communication between striatal astrocytes and ChIs, through which astrocytes can rapidly modulate excitability and downstream dopamine release at subsecond timescales. They suggest further that striatal glia-neuron interactions might offer avenues for novel strategies to modify striatal circuit function in disease states.