Electrical coupling between chromatophore muscle fibers allows for versatile control of chromatophore expansion in squid

Abstract

AbstractCamouflage color change in cephalopods is generated by the expansion and relaxation of hundreds to thousands of chromatophore pigment organs in the skin. Individual chromatophores display color when the central pigment sac is expanded to several times its original size by a ring of 20-30 radial muscles, which are electrically coupled and are innervated by multiple motoneurons. However, mechanisms for their neuromuscular control are unclear. Here we characterize chromatophore expansion kinematics and perform simultaneous whole-cell recordings on pairs of muscle fibers of a chromatophore in squid hatchlings. We show that activity is highly correlated between muscle fibers of a chromatophore due to a high ratio of electrical coupling between all muscles for slow currents. However, fast currents are filtered and decrease rapidly further away from the muscle receiving the inputs. This low-pass filtering property of electrical coupling allows fast inputs to activate one muscle while persistent inputs spread throughout the chromatophore to synchronously activate all muscles, providing a versatile mode of control for chromatophore expansion.