Structural and Functional Arrangements of Atrial Myocytes that Facilitate Excitation-Contraction Coupling

Rabbit atrial myocytes lack transverse tubules and only the peripheral sarcoplasmic reticulum (SR) is in contact with the surface membrane (junctional SR; j-SR) and exposed to Ca influx through voltage-gated sarcolemmal Ca channels that initiates Ca release which propagates centripetally by Ca-induced Ca release from non-junctional SR (nj-SR). In this study we examined the structural and functional characteristics of excitation-contraction coupling (ECC) unique to atrial myocytes. Subsarcolemmal (SS) Ca release from j-SR preceded release at central (CT) nj-SR regions, and SS release was of higher amplitude compared to CT release. Using simultaneous measurements of cytosolic ([Ca]i) and intra-SR ([Ca]SR) Ca, we show that depletions of SS [Ca]SR were smaller compared to CT [Ca]SR depletions during electrical stimulation. Atrial myocytes revealed an approximately 1-2 µm wide gap devoid of mitochondria and SR structures between the j-SR and the nj-SR that the Ca signal must traverse to activate release from nj-SR. The spread of Ca from the j-SR to the nj-SR occurred very rapidly and was aided by the absence of mitochondria which might buffer the diffusion of Ca. In contrast to SS release, the continuation of Ca release through the nj-SR to the cell center occurred much slower in a Ca wave-like fashion, and the rise of [Ca]i detected at individual release sites of the nj-SR preceded the depletion of [Ca]SR. During this latency period a transient elevation of [Ca]SR was observed that acted as an intra-SR Ca sensitization wave that may facilitate the spread of excitation through the nj-SR via the luminal Ca-sensitivity of the ryanodine receptor Ca release channel. In summary, we have identified key structural and functional characteristics of atrial myocytes that allow for efficient ECC in the intact heart.