SHAPING SENSATION: HOW MEMBRANE CURVATURE TUNES CRITICALITY IN HAIR CELLS

Many sensory organs—and perhaps some neural circuits—gain an advantage by operating near criticality: a dynamical boundary between stable behavior and chaos. Near this boundary, small inputs can be strongly amplified, boosting sensitivity and usable dynamic range. The key problem is control: how do biological systems set, and maintain, the right distance from criticality despite noise and drift?

The auditory periphery illustrates both the appeal and the puzzle. The human cochlea relies on only ~16,000 sensory hair cells, yet allows us to hear from whispers to thunderclaps while tracks vibrations at kilohertz rates. To study how a sensory receptor can be held near criticality, we use the Rana catesbeiana, where the a hair cell's proximity to criticality is easy to see: Each hair cell bears a hair bundle, a cluster of microvilli that pivots to detect vibrations, and that—when poised near criticality—oscillate spontaneously.

Here we identify a new control mechanism in which lipid-bilayer mechanics couple to lipid signaling to tune bundle dynamics. Using amphipathic compounds that reshape membrane curvature, we observe reversible shifts between quiescent and oscillatory regimes that match predictions from our theory of bilayer-mediated channel cooperativity. We then test for endogenous control and find that phospholipase C (PLC) is required: PLC perturbation shifts the operating point, and immunocytochemistry localizes PLC isoforms within hair bundles. Together, these findings support the hypothesis that PLC-dependent lipid remodeling changes bilayer forces on mechanosensitive channels, biases their gating, and thereby tunes the sensory receptor’s distance from criticality.