J Comp Physiol A (2009) 195:491–500 DOI 10.1007/s00359-009-0426-7 123 ORIGINAL PAPER Premotor nonspiking neurons regulate coupling among motoneurons that innervate overlapping muscle Wber population Mariano Julián Rodriguez · Carlos Bernardo Perez-Etchegoyen · Lidia Szczupak Received: 15 August 2008 / Revised: 9 February 2009 / Accepted: 18 February 2009 / Published online: 17 March 2009  Springer-Verlag 2009 Abstract Recent work indicated that co-activity of diVer- ent motoneurons (MNs) in the leech can be regulated through a network that is centered on a pair of nonspiking (NS) neurons. Here, we investigate whether this eVect generalizes to diVerent types of MNs that display diVerential co-activity patterns in diVerent motor behaviors: the dorsal longitudinal excitors DE-3 and the dorsal and ventral exci- tors MN-L. The data indicates that both motoneurons are coupled to the NS neurons through rectifying junctions that are activated when the motoneuron membrane potential becomes more negative than that of the NS, and that they exert an inhibitory synaptic potential on NS via a polysyn- aptic pathway. In addition, DE-3 and MN-L are linked by junctions that allow mutual excitation but the transmission of excitatory signals from MN-L to DE-3 depended on NS membrane potential. The results support the view that NS neurons can play a central role in orchestrating the co-activity of MNs during motor behaviors. Keywords Electrical coupling · Motor circuits · Leech · Rectifying junctions · Nonspiking neuron Introduction Several evidences indicate that, although motor circuits are highly hierarchical structures, the lower levels in this hier- archy play an important role in shaping motor patterns (Bizzi et al. 2000; Fetz et al. 2000; Cattaert and Le Ray 2001); interactions between premotor interneurons and motoneurons form “movement primitives” or “spinal mod- ules” (in vertebrates) responsible for the basic movement patterns that compose a motor behavior. Because of its relative simplicity, the leech has been an excellent organism to learn about the organization of motor circuits (Kristan et al. 2005). Two Wndings suggest that hori- zontal interactions among excitatory motoneurons (MNs) may play a complex role in shaping motor patterns: MNs show a high degree of coupling among themselves (Ort et al. 1974; Fan et al. 2005); and a pair of nonspiking (NS) premotor neurons are electrically coupled to all excitatory MNs through rectifying electrical junctions (active when NS membrane potential is more negative than the MN membrane potential) (Wadepuhl 1989; Rela and Szczupak 2007). Recent work indicated that co-activity of diVerent MNs can be regulated through a network that is centered on the NS neurons (Rela and Szczupak 2003). In this network, MNs are connected to NS neurons through two parallel pathways: (1) the rectifying electrical coupling between MNs and NS; and (2) excitation of MNs evoke a chemi- cally mediated inhibitory potential in NS neurons through a polysynaptic pathway. This connectivity enables NS neu- rons to regulate the co-activity between two speciWc moto- neurons, the CV motoneurons that control circular ventral muscles and the AE motoneurons that control the erection of skin annuli (Rela and Szczupak 2003). In the present work, we have investigated whether this network can be generalized to other motoneurons in the leech. SpeciWcally, we chose two excitors of longitudinal muscles: the dorsal excitor cell DE-3 that controls dorsal longitudinal muscles and the MN-L motoneuron that excites both dorsal and ventral longitudinal muscles (Stuart 1970). The interest in these particular MNs resides in the diVerential pattern of activity displayed by them in two behaviors of the leech, swimming and shortening. When M. J. Rodriguez · C. B. Perez-Etchegoyen · L. Szczupak (&) Dto de Fisiología, Biología Molecular y Celular, FCEN-UBA, IFIBYNE-CONICET, Buenos Aires, Argentina e-mail: szczupak@mail.retina.ar