Morphologic features and electrical membrane properties of projection neurons in the marginal layer of the medullary dorsal horn of the rat

Abstract

Possible correspondence between morphologic features and electrical membrane properties of projection neurons in lamina I [the marginal zone (MZ)] of the caudal subnucleus of the spinal trigeminal nucleus [the medullary dorsal horn (MDH)] was examined by using intracellular recordings and biocytin-injections combined with histochemical and immunohistochemical staining techniques. The experiments were done in horizontal slice preparations of the rat brain. Thirteen MZ neurons were recorded stably and stained successfully. These neurons were confirmed to send their axons to the brain regions outside the MDH by camera lucida reconstruction. They were divided into two types on the basis of branching patterns of their axons within the MDH: Type I projection (P-I) neurons (n = 7 neurons) had main axons that rarely emitted axon collaterals within the MDH, whereas type II projection (P-II) neurons (n = 6 neurons) had main axons that emitted many axon collaterals within laminae I, II (substantia gelatinosa), and III (magnocellular part) of the MDH and also to the spinal tract of the trigeminal nerve; these axon collaterals usually constituted a dense mesh of axonal processes within laminae I and II of the MDH, especially in lamina II. About half of the neurons of each type showed immunoreactivity for the neurokinin-1 receptor. Resting membrane potentials were significantly more positive in P-I neurons than in P-II neurons. The P-II neurons had higher input resistance, a longer membrane time constant, and a higher threshold for spike than P-I neurons. In response to weak, long depolarizing current pulses, P-II neurons often showed slow ramp depolarization; the same neurons exhibited delayed repolarization to the resting potential (slow after depolarization) after the offset of the long depolarizing current pulses. Neither the slow-ramp depolarization nor the slow after depolarization was observed in P-I neurons. Slow return to resting membrane potential after offset of hyperpolarizing current pulses also was observed frequently in P-II neurons but not in P-I neurons. The results indicate that P-II neurons differ in their membrane properties compared with P-I neurons, and P-II neurons may be involved in the local circuit mechanism within the MDH more deeply than P-I neurons.