Two components of rapid sensory adaptation in a cockroach mechanoreceptor neuron

The femoral tactile spine of the cockroach is innervated by a single sensory neuron with its cell body in the spine. A step deflection of the spine produces a burst of action potentials which decays to zero in ~ 1 s. This rapid adaptation occurs during encoding of action potentials and can be studied by extracellular electrical stimulation of the sensory neuron. The threshold current of the neuron is labile, increasing with depolarization and decreasing with mild hyperpolarization. During rapid adaptation, the threshold current increases to exceed any steady stimulating current. The dynamic behavior of the threshold current in the tactile spine neuron was observed following step changes in membrane current. The threshold current followed a trajectory which could always be well fitted by a sum of two exponential decays with time constants of ~ 100 and 1,000 ms. The amplitude of the slow component of threshold change was proportional to the size of the step change in membrane current but saturated at strong hyperpolarizations. Its time constant decreased monotonically with depolarization. In contrast, the fast component had more complex behavior, changing biphasically with step amplitude and reversing with initial hyperpolarizations. Its time constant was maximal at the resting membrane potential. The amplitude of the fast component was strongly reduced by treatment with N-chlorosuccinimide (NCS), an agent which reduces sodium channel inactivation. It was not affected by some agents known to block potassium channels. The slow component was not affected by NCS, tetraethylammonium chloride, apamin, or charybdotoxin. Approximate contributions of the two components to the steady-state threshold were reconstructed from step responses. These indicate that the slow component dominates when the receptor is hyperpolarized. However, during depolarizations from rest, as occur with normal stimulation, the two components contribute approximately equally to threshold changes.