The specific roles of the classical transient receptor potential (TRPC) channel subfamily in neuronal function are still elusive. By studying heterologously expressed TRPC1 channels we found that recombinant TRPC1 was not able to function as a homomeric channel. Instead, TRPC1 subunits form functional receptor-operated heteromeric channel complexes with TRPC3, 4, 5, 6, and 7. Heteromers containing TRPC1 subunits showed significantly decreased calcium permeation in heterologous cell systems. Mutation of amino acids in the putative pore forming region of TRPC1 further reduced calcium permeability. In immortalized gonadotropin releasing hormone (GnRH) expressing neuronal cells endogenously expressing TRPC1, 2, 4, 5, and 6, downregulation of TRPC1 by siRNA results in increased basal cytosolic calcium concentrations and elevated calcium permeability. We found no evidence for an involvement of TRPC1 in store-operated cation influx in these cells. Moreover, TRPC1 suppressed the migration of GnRH neurons without affecting cell proliferation. These findings suggest that TRPC1 is able to form heteromeric TRPC channel complexes giving rise to reduced calcium permeability thereby restricting neuronal cell migration.