Ca²⁺ influx through L-type Ca_v1.2 (_1C) Ca²⁺ channels is a critical step in the activation of cardiac ryanodine receptors (RyRs) and release of Ca²⁺ (CICR). The released Ca²⁺, in turn, is the dominant determinant of inactivation of Ca²⁺ current (I_Ca), and termination of release. Although Ca²⁺ cross-signaling is mediated by high Ca²⁺ fluxes in the micro domains of _1C/RyR complexes, I_Ca gated Ca²⁺ cross-signaling is surprisingly resistant to intracellular Ca²⁺ buffering, and has steeply voltage-dependent gain, inconsistent with a strict CICR mechanism, suggesting additional regulatory step(s). To explore possible regulatory role of carboxyl- (C-) terminal tail of _1C in modulating Ca²⁺ signaling, we tested the effects of introducing two _1C C-terminal peptides, LA (1571-1599) and K (1617-1636) on the central _1C- unassociated Ca²⁺ release sites of atrial myocytes, using rapid (240 Hz) two-dimensional confocal Ca²⁺ imaging. The frequency of spontaneously activating central sparks increased by ~4 fold on dialyzing LA-, but not K-peptide into myocytes voltage- clamped at -80 mV. The rate but not the magnitude of caffeine (10 mM)-triggered central Ca²⁺ release was significantly accelerated by LA- but not K- peptide. Individual Ca²⁺ spark size and flux were larger in LA-, but not in K-peptide dialyzed myocytes. Although LA-peptide did not change the amplitude or inactivation kinetics of I_Ca, LA- peptide did strongly enhance the central Ca²⁺ transients triggered by I_Ca at -30 (small I_Ca) but not at +20 mV (large I_Ca). In contrast, K-peptide had no effects on either I_Ca or local Ca²⁺ transients. LA-peptide with deleted calmodulin-binding region (LM1-peptide) had no significant effects on the central spark frequency but suppressed spontaneous spark frequency in the periphery. Our results indicate that calmodulin-binding LA motif of the _1C C-terminal tail may sensitize the RyRs, thereby increasing their open probability and providing for both the voltage-dependence of CICR and the higher frequency of spark occurrence in the periphery of atrial myocytes where the native _1C/RyR complexes are intact.