Receptor Potentials and Electrical Properties of Nonspiking Stretch-Receptive Neurons in the Sand Crab Emerita analoga (Anomura, Hippidae)

Abstract

Receptor potentials and electrical properties of nonspiking stretch-receptive neurons in the sand crab Emerita analoga (Anomura, Hippidae). Four nonspiking, monopolar neurons with central somata and large peripheral dendrites constitute the sole innervation of the telson-uropod elastic strand stretch receptor in Emerita analoga. We characterized their responses to stretch and current injection, using two-electrode current clamp, in intact cells and in two types of isolated peripheral dendritic segments, one that included and one that excluded the dendritic termini (mechanosensory membrane). The membrane potentials of intact cells at rest (mean ± SD: −57 ± 4.4 mV, n = 30), recorded in peripheral or neuropil processes, are similar to the membrane potentials of isolated dendritic segments and always less negative than membrane potentials of motoneurons and interneurons recorded in the same preparations. Ion substitution experiments indicate that the membrane potential is influenced strongly by Na+ conductance, probably localized in the mechanotransducing terminals within the elastic strand. The form of the receptor potential in response to ramp-hold-release stretch remains the same as stretch amplitude is varied and is not dependent on initial membrane potential (−70 to −30 mV) or recording site: initial depolarization (slope follows ramp of applied stretch), terminated by rapid, partial repolarization to a plateau (delayed depolarization) that is intermediate between the peak depolarization and the initial potential and sustained for the duration of the stretch. Responses to depolarizing current pulses are similar to stretch-evoked receptor potentials, except for small amplitude stimuli: an initial peak occurs only in response to stretch and probably reflects elastic recoil of the extracellular matrix surrounding the dendritic terminals. The rapid, partial repolarization depends on holding potential and is abolished by 4-aminopyridine (4-AP; 10 mM), implicating a fast-activating, fast-inactivating K+ conductance; TEA (60 mM) abolishes the remaining slow repolarization to the plateau. In intact cells, but not dendritic segments, regenerative depolarizations can arise in response to stretch or depolarizing current pulses; they are reduced by CdCl2 (10 μM) in the saline containing TEA and 4-AP and probably reflect current spread from Ca2+ influx at presynaptic terminals in the ganglion. We found no evidence for other voltage-activated conductances. Unlike morphologically similar “nonspiking” thoracic receptors of other species, E. analoga’s nonspiking neurons are electrically compact and do not boost the analogue afferent signal by voltage-activated inward currents. The most prominent (only?) voltage-activated extra-ganglionic conductances are for potassium; by reducing the slope of the stretch-plateau depolarization curve, they extend each neuron’s functional range to the full range of sensitivity of the receptor.