•  Burst firing activities are effective for the release of neuropeptides from peptidergic neurones. •  A peptidergic neurone, the terminal nerve (TN)‐gonadotrophin releasing hormone (GnRH) neurone, shows spontaneous burst firing activities only infrequently. •  Only a single pulse electrical stimulation of the neuropil surrounding the TN‐GnRH neurones induces transient burst activities in TN‐GnRH neurones via cholinergic mechanisms. •  The activation of muscarinic acetylcholine receptors results in a long‐lasting hyperpolarisation, inducing rebound burst activities in TN‐GnRH neurones. •  These new findings suggest a novel type of cholinergic regulation of burst activities in peptidergic neurones, which should contribute to the release of neuropeptides. Abstract  Peptidergic neurones play a pivotal role in the neuromodulation of widespread areas in the nervous system. Generally, it has been accepted that the peptide release from these neurones is regulated by their firing activities. The terminal nerve (TN)‐gonadotrophin releasing hormone (GnRH) neurones, which are one of the well‐studied peptidergic neurones in vertebrate brains, are characterised by their spontaneous regular pacemaker activities, and GnRH has been suggested to modulate the sensory responsiveness of animals. Although many peptidergic neurones are known to exhibit burst firing activities when they release the peptides, TN‐GnRH neurones show spontaneous burst firing activities only infrequently. Thus, it remains to be elucidated whether the TN‐GnRH neurones show burst activities and, if so, how the mode switching between the regular pacemaking and bursting modes is regulated in these neurones. In this study, we found that only a single pulse electrical stimulation of the neuropil surrounding the TN‐GnRH neurones reproducibly induces transient burst activities in TN‐GnRH neurones. Our combined physiological and morphological data suggest that this phenomenon occurs following slow inhibitory postsynaptic potentials mediated by cholinergic terminals surrounding the TN‐GnRH neurones. We also found that the activation of muscarinic acetylcholine receptors induces persistent opening of potassium channels, resulting in a long‐lasting hyperpolarisation. This long hyperpolarisation induces sustained rebound depolarisation that has been suggested to be generated by a combination of persistent voltage‐gated Na+ channels and low‐voltage‐activated Ca2+ channels. These new findings suggest a novel type of cholinergic regulation of burst activities in peptidergic neurones, which should contribute to the release of neuropeptides.