1. In turtle Purkinje cells in vitro successive climbing fibre responses (CFRs) gradually induced a hyperpolarization that persisted with maintained stimulation and decayed over minutes after climbing fibre stimulation was terminated. 2. The rate of development and the amplitude of this long‐lasting hyperpolarization (LHP) increased with the frequency of CFRs. 3. The LHP was also induced by Ca2+ spikes evoked by current injection but not by Na+ spikes. The LHP was blocked by Co2+ but not by tetrodotoxin and could not be explained solely by an increased K+ conductance. 4. Depolarizing current during a train of CFRs enhanced the regenerative component of CFRs and promoted the LHP. Hyperpolarizing current during the stimulus train reduced the regenerative component of CFRs and attenuated the resulting LHP. 5. In the range of membrane potentials attained at different levels of climbing fibre activity the regenerative component of CFRs varied from being dominant at very low stimulus frequency (0.1 s‐1) to being inconspicuous at high stimulus frequency (10 s‐1). 6. It is concluded that successive CFRs induce a Ca2+‐dependent, long‐lasting hyperpolarization. The magnitude of the hyperpolarization is regulated by the rate of CFRs and by the voltage‐ and frequency‐dependent configuration of each individual CFR. 7. The active, non‐synaptic properties of turtle Purkinje cells make the Ca2+ influx during climbing fibre responses prone to regulation by on‐going synaptic activity and by the after‐effects of synaptic activity on a time scale of minutes. We suggest that this arrangement may enhance the capacity and complexity of spatial and temporal synaptic integration in Purkinje cells.