Modulation of an Integrated Central Pattern Generator–Effector System: Dopaminergic Regulation of Cardiac Activity in the Blue CrabCallinectes sapidus

Abstract

Fort, Timothy J., Vladimir Brezina, and Mark W. Miller. Modulation of an integrated central pattern generator-effector system: dopaminergic regulation of cardiac activity in the blue crab Callinectes sapidus. J Neurophysiol 92: 3455-3470, 2004; doi:10.1152/ jn.00550.2004. Theoretical studies have suggested that the output of a central pattern generator (CPG) must be matched to the properties of its peripheral effector system to ensure production of functional behavior. One way that such matching could be achieved is through coordinated central and peripheral modulation. In this study, morphological and physiological methods were used to examine the sources and actions of dopaminergic modulation in the cardiac system of the blue crab, Callinectes sapidus. Immunohistochemical localization of tyrosine hydroxylase (TH) revealed a prominent neuron in the commissural ganglion, the L-cell, that projected a large-diameter axon to the pericardial organ (PO) by an indirect and circuitous route. Within the PO, the L-cell axon gave rise to fine varicose fibers, suggesting that it releases dopamine in a neurohormonal fashion onto the heart musculature. In addition, one branch of the axon continued beyond the PO to the heart, where it innervated the anterior motor neurons and the posterior pacemaker region of the cardiac ganglion (CG). In physiological experiments, exogenous dopamine produced multiple effects on contraction and motor neuron burst parameters that corresponded to the dual central-peripheral modulation suggested by the L-cell morphology. Interestingly, parameters of the ganglionic motor output were modulated differently in the isolated CG and in a novel semiintact system where the CG remained embedded within the heart musculature. These observations suggest a critical role of feedback from the periphery to the CG and underscore the requirement for integration of peripheral (neurohormonal) actions and direct ganglionic modulation in the regulation of this exceptionally simple system.

A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

“…Given the sensitivity of MCN1 and CPN2 to relatively brief POC stimulation, there may well be times when this input acts largely or exclusively as a local modulator of neuronal activity, whereas at other times its activation results in both paracrine and endocrine actions. Previous studies in other systems have established the ability of the same neurons to release signaling molecules that act both locally, in a paracrine fashion, and as circulating hormones (Mayeri, 1979;Sigvardt et al, 1986;Jung and Scheller, 1991;Loechner and Kaczmarek, 1994;Ludwig and Pittman, 2003;Fort et al, 2004;Oliet et al, 2007).…”

Distinct or shared actions of peptide family isoforms: I. Peptide-specific actions of pyrokinins in the lobster cardiac neuromuscular system

“…Christie, 2011;Christie et al, 2010a). Local sources of neuromodulators include the cardiac pacemaker and motor neurons themselves [glutamate in the former (Delgado et al, 2000) and a member of the calcitonin-like diuretic hormone/diuretic hormone 31 peptide family in the latter (Christie et al, 2010b)], and axons of projection neurons whose somata are located elsewhere in the nervous system (Cooke, 2002), which are the local sources of at least GABA (Delgado et al, 2000) and dopamine (Fort et al, 2004). The neuroendocrine pericardial organ, which surrounds the heart and the X-organ-sinus gland (XO-SG) complex, located in the eyestalks, are the primary sources of the hemolymph-borne neuromodulators that influence the cardiac CPG-effector system (Christie, 2011).…”

Forces generated during stretch in the heart of the lobsterHomarus americanusare anisotropic and are altered by neuromodulators

“…The signals from the force transducers were amplified by a Model 44 Brownlee Precision Instrumentation amplifier and recorded with a Cambridge Electronic Design (CED) Micro 1401 digitizer paired with Spike2 version 7.03 software (CED, Cambridge, UK). The output of the force transducer is reported in grams rather than Newtons for consistency with other studies that have studied single locations on the length-tension curve (Fort et al, 2004(Fort et al, , 2007aStevens et al, 2009;Christie et al, 2010b;Dickinson et al, 2015).…”

“…Although the effects of neuromodulators on crustacean CPGeffector systems are well documented, these studies have only examined the physiological effects at single locations on the lengthtension curve (Mercier and Russenes, 1992;Fort et al, 2004;Wilkens et al, 2005;Fort et al, 2007a,b;Stevens et al, 2009;Christie et al, 2010b;Dickinson et al, 2015). However, it is important to consider the functional space in which the neurotransmitters are working.…”