The neuronal L-type calcium channels (LTCCs) Ca_v1.2α1 and Ca_v1.3α1 are functionally distinct. Ca_v1.3α1 activates at lower voltages and inactivates more slowly than Ca_v1.2α1, making it suitable to support sustained L-type Ca²⁺ inward currents (I_Ca,L) and serve in pacemaker functions. We compared the biophysical and pharmacological properties of human retinal Ca_v1.4α1 using the whole-cell patch-clamp technique after heterologous expression in tsA-201 cells with other L-type α1 subunits. Ca_v1.4α1-mediated inward Ba²⁺ currents (I_Ba) required the coexpression of α2δ1 and β3 or β2a subunits and were detected in a lower proportion of transfected cells than Ca_v1.3α1. I_Ba activated at more negative voltages (5% activation threshold; -39mV; 15 mm Ba²⁺) than Ca_v1.2α1 and slightly more positive than Ca_v1.3α1. Voltage-dependent inactivation of I_Ba was slower than for Ca_v1.2α1 and Ca_v1.3α1(∼50% inactivation after 5 sec; α2δ1 + β3 coexpression). Inactivation was not increased with Ca²⁺ as the charge carrier, indicating the absence of Ca²⁺-dependent inactivation. Ca_v1.4α1 exhibited voltage-dependent, G-protein-independent facilitation by strong depolarizing pulses. The dihydropyridine (DHP)-antagonist isradipine blocked Ca_v1.4α1 with ∼15-fold lower sensitivity than Ca_v1.2α1 and in a voltage-dependent manner. Strong stimulation by the DHP BayK 8644 was found despite the substitution of an otherwise L-type channel-specific tyrosine residue in position 1414 (repeat IVS6) by a phenylalanine. Ca_v1.4α1 + α2δ1 + β channel complexes can form LTCCs with intermediate DHP antagonist sensitivity lacking Ca²⁺-dependent inactivation. Their biophysical properties should enable them to contribute to sustained I_Ca,L at negative potentials, such as required for tonic neurotransmitter release in sensory cells and plateau potentials in spiking neurons.