Osteoclasts are multinucleated bone-resorbing cells that show structural and functional differences between the resorbing and non-resorbing (motile) states during the bone resorption cycle. In the present study, we measured intracellular Ca²⁺ concentration ([Ca²⁺]_i) in non-resorbing versus resorbing rat osteoclasts. Basal [Ca²⁺]_i in osteoclasts possessing pseudopodia (non-resorbing/motile state) was around 110 nM and significantly higher than that in actin ring forming osteoclasts (resorbing state, around 50 nM). In non-resorbing/motile osteoclasts, exposure to high-K⁺ reduced [Ca²⁺]_i, whereas high-K⁺ increased [Ca²⁺]_i in resorbing state osteoclasts. In non-resorbing/motile cells, membrane depolarization and hyperpolarization applied by the patch-clamp technique decreased and increased [Ca²⁺]_i, respectively. Removal of extracellular Ca²⁺ or application of 300 µM La³⁺ reduced [Ca²⁺]_i to about 50 nM in non-resorbing/motile osteoclasts and high-K⁺-induced reduction of [Ca²⁺]_i could not be observed under these conditions. Neither inhibition of intracellular Ca²⁺ stores or plasma membrane Ca²⁺pumps nor blocking of L- and N-type Ca²⁺ channels significantly reduced [Ca²⁺]_i. Exposure to high-K⁺ inhibited the motility of non-resorbing osteoclasts and reduced the number of actin rings and pit formation in resorbing osteoclasts. These results indicate that in non-resorbing/motile osteoclasts, a La³⁺-sensitive Ca²⁺ entry pathway is continuously active under resting conditions, keeping [Ca²⁺]_i high. Changes in membrane potential regulate osteoclastic motility by controlling the net amount of Ca²⁺ entry in a "reversed" voltage-dependent manner; i.e., depolarization decreases and hyperpolarization increases intracellular [Ca²⁺]_i.