MEMBRANE TENSION IN SWELLING AND SHRINKING MOLLUSCAN NEURONS

When neurons undergo dramatic shape and volume changes, how is surface area adjusted appropriately? The membrane tension hypothesis-namely t hat high tensions favor recruitment of membrane to the surface whereas low tensions favor retrieval-provides a simple conceptual framework f or surface area homeostasis. With membrane tension and area in a feedb ack loop, tension extremes may be averted even during excessive mechan ical load variations. We tested this by measuring apparent membrane te nsion of swelling and shrinking Lymnaea neurons. With hypotonic medium (50%), tension that was calculated from membrane tether forces increa sed from 0.04 to as much as 0.4 mN/m, although at steady state, swolle n-cell tension (0.12 mN/m) exceeded controls only threefold. On reshri nking in isotonic medium, tension reduced to 0.02 mN/m, and at the sub stratum, membrane invaginated, creating transient vacuole-like dilatio ns. Swelling increased membrane tension with or without BAPTA chelatin g cytoplasmic Ca2+, but with BAPTA, unmeasurably large (although not l ytic) tension surges occurred in approximately two-thirds of neurons. Furthermore, in unarborized neurons voltage-clamped by perforated-patc h in 50% medium, membrane capacitance increased 8%, which is indicativ e of increasing membrane area. The relatively damped swelling-tension responses of Lymnaea neurons (no BAPTA) were consistent with feedback regulation. BAPTA did not alter resting membrane tension, but the larg e surges during swelling of BAPTA-loaded neurons demonstrated that 50% medium was inherently treacherous and that tension regulation was imp aired by subnormal cytoplasmic [Ca2+]. However, neurons did survive te nsion surges in the absence of Ca2+ signaling. The mechanism to avoid high tension rupture may be the direct tension-driven recruitment of m embrane stores.