Electrical Coupling between Locomotor-Related Excitatory Interneurons in the Mammalian Spinal Cord

Abstract

Locomotor rhythm generation is a fundamental characteristic of neural networks in the spinal cord. Identifying the synaptic interactions between neurons in the locomotor circuitry is key to our understanding of the mechanisms that underlie the production of rhythmic motor outputs. Using transgenic mice in which the homeobox gene HB9 drives the reporter green fluorescent protein (GFP), we have demonstrated that a genetically distinct cluster of Hb9/GFP-expressing interneurons (Hb9 INs) can generate locomotor-like rhythms in the newborn mouse spinal cord (Hinckley et al., 2005b). Processes of Hb9 INs are in close apposition to adjacent Hb9 INs, raising the possibility that the interneurons are synaptically interconnected. To test this hypothesis, whole-cell paired recordings were performed from visually identified Hb9 INs. High-incidence bidirectional electrical coupling was evident between Hb9 INs in spinal cords of newborn and juvenile mice. The coupling strength varied from 2 to 32% with an average of 12%. Our data suggested that the variability was not correlated with the distribution of electrical synapses at different electronic distances. Electrical synapses behaved as low-pass filters, reducing currents passing at frequencies >3 Hz. Episodes of spontaneous bursts of EPSCs were synchronous in coupled Hb9 INs, indicating that common synaptic inputs coordinated their activity. However, non-NMDA receptor-mediated synaptic transmission was not required to synchronize neurochemically induced membrane oscillations between electrically coupled interneurons. The finding that electrical transmission persists in mice that can walk is indicative of its importance in coordinating the activity of this neuronal population in functionally mature spinal networks.