Developmental changes in the electrophysiological properties of brain stem trigeminal neurons during pattern (barrelette) formation.

Abstract

In the brain stem trigeminal nuclei of rodents there is a patterned representation of whiskers and sinus hairs. The subnucleus interpolaris (SPI) contains the largest and the most conspicuous whisker patterns (barrelettes). Although neural activity plays a role in pattern formation, little is known about the electrophysiological properties of developing barrelette neurons. Here we examined the functional state of early postnatal SPI neurons during and after the consolidation of patterns by using in vitro intracellular recording techniques. After the consolidation of barrelettes [>/= postnatal day (P)4], responses to intracellular current injection consistently reflected the activation of a number voltage-dependent conductances. Most notable was a mixed cation conductance (IH) that prevented strong hyperpolarization and a large low-threshold Ca2+ conductance, which led to Ca2+ spikes and burst firing. At the oldest ages tested (P11-P14) some cells also exhibited an outward K+ conductance (IA), which led to significant delays in action-potential firing. Between P0-3, a time when the formation of barrelettes in the brain stem is still susceptible to damage of the sensory periphery, cells responded linearly to intracellular current injection, indicating they either lacked such voltage-gated properties or weakly expressed them. At all ages tested (P0-14), SPI cells were capable of generating trains of action potentials in response to intracellular injection of depolarizing current pulses. However, during the first few days of postnatal life, spikes were shorter and longer. Additionally, spike trains rose more linearly with stimulus intensity and showed frequency accommodation at early ages. Taken together, these results indicate that the electrophysiological properties of SPI neurons change markedly during the period of barrelette consolidation. Moreover, the properties of developing SPI neurons may play a significant role in pattern formation by minimizing signal distortion and ensuring that excitatory responses from sensory periphery are accurately received and transmitted according to stimulus strength.