The molecular identity of non-Ca_v1.3 channels in auditory and vestibular hair cells has remained obscure, yet the evidence in support of their roles as adjuvant to Ca_v1.3 channels to promote diverse Ca²⁺-dependent functions is undisputable. Recently, a transient Ca_v3.1 current that serves as a functional signature for the development and regeneration of hair cells have been identified in the chicken basilar papilla. The Ca_v3.1 current promotes spontaneous activity of the developing hair cell, which may be essential for synapse formation. Here, we have isolated and sequenced the full-length cDNA of a distinct isoform of Ca_v3.1 in the mouse inner ear. The channel is derived from alternative splicing of exon14, exon25A, exon34 and exon35. Functional expression of the channel in Xenopus oocytes yielded Ca²⁺ currents, which have a permeation phenotype consistent with T-type channels. However, unlike most multi-ion channels, the T-type channel does not exhibit the anomalous mole fraction effect (AMFE); a finding that may ensue from comparable permeation properties of divalent cations. The Cav3.1 channel was expressed in sensory and non-sensory epithelia of the inner ear. Moreover, there are profound changes in the expression levels during development. The differential expression of the channel during development and the distinct pharmacology of the inner ear-specific Ca_v3.1 channel that may have contributed to the difficulties associated with identification of the non-Ca_v1.3 currents.