The lateral habenula (LHb) is a key brain structure that receives input from higher brain regions and regulates monoaminergic activity. LHb hyperactivity has been implicated in the pathophysiology of depression, but the electrophysiological mechanisms underlying this hyperactivity remain poorly understood. To address this issue, we investigated how chronic stress alters the firing properties of LHb neurons in a mouse model of chronic social defeat. Whole-cell recordings were conducted from LHb neurons in the mouse acute brain slices. LHb neurons exhibited two types of rebound depolarizing potentials (RDPs) after the offset of hyperpolarization: short-RDPs (lasting <400 ms) and long-RDPs (order of seconds). Stress-susceptible mice showed a significantly reduced occurrence of long-RDPs, whereas spike firing in response to depolarizing current injections remained unchanged. Both short- and long-RDPs were triggered by T-type voltage-dependent Ca2+ channels and shortened by small-conductance Ca2+-activated K+ (SK) channels. The prolonged depolarizing phase of long-RDPs was mediated by cyclic nucleotide-gated (CNG) channels, which were activated via electrical coupling formed between neurons and non-neuronal cells. Whole-cell recording using an internal solution including a gap junction-permeable dye revealed that neurons formed dye coupling with non-neuronal cells, including oligodendrocytes and/or oligodendrocyte precursor cells. RNA-sequencing and genome editing experiments suggested that Cnga4, a CNG channel subtype, was the primary candidate for the long depolarizing phase of long-RDP, and its expression was decreased in the stress-susceptible mice. These findings suggest that stress-dependent changes in the firing activity of neurons are regulated by neuron-non-neuron networks formed in the LHb. KEY POINTS: Mouse lateral habenular (LHb) neurons exhibit short (<400 ms) rebound depolarizing potentials (short-RDPs) or long-RDPs (order of seconds) (long-RDPs) after the offset of hyperpolarization. The incidence of long-RDP neurons is significantly reduced in mice susceptible to chronic social defeat stress. The long depolarizing phase of long-RDPs is mediated by cyclic nucleotide-gated (CNG) channels, which are activated in non-neuronal cells via gap junctions. The expression of Cnga4, the gene encoding a subtype of the CNG channel, is decreased in the stress-susceptible mice. These results help us understand the mechanisms underlying stress-induced electrophysiological changes in LHb neurons and the functional roles of neuron-non-neuron networks for these neurons.