Projection Neurons with Shared Cotransmitters Elicit Different Motor Patterns from the Same Neural Circuit

Abstract

Specificity in the actions of different modulatory neurons is often attributed to their having distinct cotransmitter complements. We are assessing the validity of this hypothesis with the stomatogastric nervous system of the crab Cancer borealis. In this nervous system, the stomatogastric ganglion (STG) contains a multifunctional network that generates the gastric mill and pyloric rhythms. Two identified projection neurons [modulatory proctolin neuron (MPN) and modulatory commissural neuron 1 (MCN1)] that innervate the STG and modulate these rhythms contain GABA and the pentapeptide proctolin, but only MCN1 contains Cancer borealis tachykinin-related peptide (CabTRP Ia). Selective activation of each projection neuron elicits different rhythms from the STG. MPN elicits only a pyloric rhythm, whereas MCN1 elicits a distinct pyloric rhythm as well as a gastric mill rhythm. We tested the degree to which CabTRP Ia distinguishes the actions of MCN1 and MPN. To this end, we used the tachykinin receptor antagonist Spantide I to eliminate the actions of CabTRP Ia. With Spantide I present, MCN1 no longer elicited the gastric mill rhythm and the resulting pyloric rhythm was changed. Although this rhythm was more similar to the MPN-elicited pyloric rhythm, these rhythms remained different. Thus, CabTRP Ia partially confers the differences in rhythm generation resulting from MPN versus MCN1 activation. This result suggests that different projection neurons may use the same cotransmitters differently to elicit distinct pyloric rhythms. It also supports the hypothesis that different projection neurons use a combination of strategies, including using distinct cotransmitter complements, to elicit different outputs from the same neuronal network.

Convergent Motor Patterns from Divergent Circuits

“…3C). These rhythms were further similar in that the protractor GM neurons and the retractor AM neuron were either silent or weakly active during these rhythms (Coleman, 1995;Wood et al, 2000;Saideman et al, 2007). In contrast, the GM and AM neurons are consistently and strongly active in the other previously characterized gastric mill rhythms (Fig.…”

“…The possibility of convergence in the LG neuron is supported by the fact that several neuropeptides, including CabTRP Ia and proctolin, have convergent actions on the same voltage-dependent current in C. borealis pyloric circuit neurons Marder, 2000, 2001). Moreover, the transmitter-mediated actions of MCN1 on LG result entirely from CabTRP Ia (Wood et al, 2000). The ionic current(s) influenced by the CabPKs remain to be determined.…”

“…In contrast, the PK peptide is present constantly when it is superfused to activate the gastric mill rhythm (Saideman et al, 2007). It is noteworthy that despite some MCN1 actions being slow modulatory influences, such as its excitation of the LG and DG neurons, these influences decay within seconds when MCN1 is either synaptically inhibited or its stimulation is terminated (Coleman and Nusbaum, 1994;Coleman et al, 1995;Bartos and Nusbaum, 1997;Wood et al, 2000). This relatively fast decay is pivotal to LG burst termination during each cycle of this rhythm .…”

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

“…Experiments in which either MCN1 or CPN2 was removed selectively suggest that the relative contributions of these two projection neurons to the VCN-elicited gastric mill rhythm reflect their previously characterized actions on gastric mill neurons. The contribution of MCN1 includes a modulatory excitation of some neurons (e.g., LG, DG) and ionotropic excitation of others (e.g., Int1) Coleman et al, 1995;Wood et al, 2000). These actions contribute to the ability of MCN1 stimulation to drive the gastric mill rhythm (Coleman et al, 1995;Bartos et al, 1999).…”

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.…”