Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network

Abstract

Distinct motor patterns are selected from a multifunctional neuronal network by activation of different modulatory projection neurons. Subsets of these projection neurons can contain the same neuromodulator(s), yet little is known about the relative influence of such neurons on network activity. We have addressed this issue in the stomatogastric nervous system of the crab Cancer borealis. Within this system, there is a neuronal network in the stomatogastric ganglion (STG) that produces many versions of the pyloric and gastric mill rhythms. These different rhythms result from activation of different projection neurons that innervate the STG from neighboring ganglia and modulate STG network activity. Three pairs of these projection neurons contain the neuropeptide proctolin. These include the previously identified modulatory proctolin neuron and modulatory commissural neuron 1 (MCN1) and the newly identified modulatory commissural neuron 7 (MCN7). We document here that each of these neurons contains a unique complement of cotransmitters and that each of these neurons elicits a distinct version of the pyloric motor pattern. Moreover, only one of them (MCN1) also elicits a gastric mill rhythm. The MCN7-elicited pyloric rhythm includes a pivotal switch by one STG network neuron from playing a minor to a major role in motor pattern generation. Therefore, modulatory neurons that share a peptide transmitter can elicit distinct motor patterns from a common target network.

Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

“…Previous work showed that the VCN mechanosensory system influences at least four CoG projection neurons . All four of these neurons have synaptic actions on gastric mill neurons Norris et al, 1994Norris et al, , 1996Blitz et al, 1999). In the current study we demonstrate that, despite these relatively widespread VCN actions, the conjoint activity of MCN1 and CPN2 is necessary and likely sufficient to mediate the VCN-elicited gastric mill rhythm.…”

“…At the onset of each experiment the neurons were identified by using routine methods described previously (Beenhakker et al, 2004). Briefly, neurons were identified by their patterns of activity, interactions with other neurons, and axonal branching patterns (Weimann et al, 1991;Norris et al, 1994;Blitz and Nusbaum, 1997;Blitz et al, 1999). All but one gastric mill circuit neuron [interneuron 1 (Int1] in the STG are also motor neurons that project via the posterior STG nerves to innervate their target muscles.…”

“…MCN1 has excitatory actions on all gastric mill circuit neurons, including the gastropyloric IC and ventricular dilator (VD) neurons Coleman et al, 1995;Bartos and Nusbaum, 1997;Blitz et al, 1999;Beenhakker, 2004) (Fig. 1 B).…”

“…In C. borealis alone there are at least five projection neurons that elicit different pyloric rhythms when individually stimulated (Norris et al, 1996;Blitz et al, 1999;Christie et al, 2004). With this in mind, sensory regulation of a neuronal circuit could result from its activation of a single projection neuron, a subset of relevant projection neurons, or all relevant projection neurons.…”

The Neuromuscular Junctions of the Slow and the Fast Excitatory Axon in the Closer of the CrabEriphia spinifronsAre Endowed with Different Ca2+Channel Types and Allow Neuron-Specific Modulation of Transmitter Release by Two Neuropeptides

“…One strategy of achieving specificity in this modulation is the colocalization of peptides with classic transmitters and the release of distinct cotransmitter complements (Blitz et al, 1999;Wood et al, 2000) (for review, see Nusbaum et al, 2001). Another strategy of achieving specificity in peptidergic actions is the axon typespecific modulation of the efficacy of discharge patterns of motor neurons at the target cells.…”