Two Neuropeptides Colocalized in a Command-Like Neuron Use Distinct Mechanisms to Enhance Its Fast Synaptic Connection

Abstract

In many neurons more than one peptide is colocalized with a classical neurotransmitter. The functional consequence of such an arrangement has been rarely investigated. Here, within the feeding circuit of Aplysia, we investigate at a single synapse the actions of two modulatory neuropeptides that are present in a cholinergic interneuron. In combination with previous work, our study shows that the command-like neuron for feeding, CBI-2, contains two neuropeptides, feeding circuit activating peptide (FCAP) and cerebral peptide 2 (CP2). Previous studies showed that high-frequency prestimulation or repeated stimulation of CBI-2 increases the size of CBI-2 to B61/62 excitatory postsynaptic potentials (EPSPs) and shortens the latency of firing of neuron B61/62 in response to CBI-2 stimulation. We find that both FCAP and CP2 mimic these two effects. The variance method of quantal analysis indicates that FCAP increases the calculated quantal size (q) and CP2 increases the calculated quantal content (m) of EPSPs. Since the PSP amplitude represents the product of q and m, the joint action of the two peptides is expected to be cooperative. This observation suggests a possible functional implication for multiple neuropeptides colocalized with a classical neurotransmitter in one neuron.

Composite Modulatory Feedforward Loop Contributes to the Establishment of a Network State

“…In particular, these studies highlighted the essential roles of peptides in input neurons that are extrinsic to the CPG network. Specifically, other than the earlier peptide localization to motoneurons (Weiss et al 1992), neuropeptides appear to be most prominently localized in input neurons that act on the CPG, i.e., sensory neurons (Furukawa et al 2001;Miller et al 1994;Vilim et al 2010), higher-order interneurons (Koh et al 2003;Morgan et al 2002;Sweedler et al 2002), as well as nerve fibers, such as apNPY, SCP, and RFamide in the EN; but are largely absent in CPG neurons. A similar situation may be present in the stomatogastric nervous system (Marder and Bucher 2007;Nusbaum et al 2001).…”

“…Recent work indicates that the Aplysia feeding network is advantageous for studying central peptidergic modulation in the context of network multifunctionality Jing et al 2007;Koh and Weiss 2007;Koh et al 2003;Morgan et al 2002;Proekt et al 2005;Sasaki et al 2009;Sweedler et al 2002;Vilim et al 2010). In particular, these studies highlighted the essential roles of peptides in input neurons that are extrinsic to the CPG network.…”

Identification of a New Neuropeptide Precursor Reveals a Novel Source of Extrinsic Modulation in the Feeding System ofAplysia

“…In Aplysia, each cycle of the feeding motor program begins with the radula protraction phase, followed by the radula retraction phase Hurwitz et al, , 1997Weiss, 2001, 2002;Morgan et al, 2002;Koh et al, 2003;Proekt and Weiss, 2003;Proekt et al, 2004). The radula protraction phase was defined to be coincident with the burst of electrical activity in the I2 nerve Hurwitz et al, , 1997.…”

“…Furthermore, multiple neuropeptides often converge to modulate the very same processes. In this respect, one of the best-studied preparations is the Aplysia feeding system, in which a number of novel neuropeptides have been identified (Cropper et al, 1987a(Cropper et al, ,b, 1988(Cropper et al, , 1994Church and Lloyd, 1991;Church et al, 1993;Brezina et al, 1995Brezina et al, , 1996Vilim et al, 1996Vilim et al, , 2000Evans et al, 1999;Hurwitz et al, 2000;Morgan et al, 2000Morgan et al, , 2002Jing and Weiss, 2001;Sweedler et al, 2002;Koh et al, 2003).…”

Neural Analog of Arousal: Persistent Conditional Activation of a Feeding Modulator by Serotonergic Initiators of Locomotion

“…Food-induced arousal in Aplysia is mediated by the serotonergic MCCs (Weiss et al, 1978;Rosen et al, 1989;Proekt and Weiss, 2003) and peptidergic feeding interneurons (Morgan et al, 2000;Koh et al, 2003;Proekt et al, 2004Proekt et al, , 2007. Here, we demonstrate that CC9 -10 function as both initiators and modulators of locomotion.…”