Summary
The muscles of the pyloric region of the stomach of the crab,Cancer borealis, are innervated by motorneurons found in the stomatogastric ganglion (STG). Electrophysiological recording and stimulating techniques were used to study the detailed pattern of innervation of the pyloric region muscles. Although there are two Pyloric Dilator (PD) motorneurons in lobsters, previous work reported four PD motorneurons in the crab STG (Dando et al. 1974; Hermann 1979a, b). We now find that only two of the crab PD neurons innervate muscles homologous to those innervated by the PD neurons in the lobster,Panulirus interrruptus. The remaining two PD neurons innervate muscles that are innervated by pyloric (PY) neurons inP. interruptus. The innervation patterns of the Lateral Pyloric (LP), Ventricular Dilator (VD), Inferior Cardiac (IC), and PY neurons were also determined and compared with those previously reported in lobsters. Responses of the muscles of the pyloric region to the neurotransmitters, acetylcholine (ACh) and glutamate, were determined by application of exogenous cholinergic agonists and glutamate. The effect of the cholinergic antagonist, curare, on the amplitude of the excitatory junctional potentials (EJPs) evoked by stimulation of the pyloric motor nerves was measured. These experiments suggest that the differences in innervation pattern of the pyloric muscles seen in crab and lobsters are also associated with a change in the neurotransmitter active on these muscles. Possible implications of these findings for phylogenetic relations of decapod crustaceans and for the evolution of neural circuits are discussed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- ACh :
-
acetylcholine
- Carb :
-
carbamylcholine
- cpv :
-
muscles of the cardio-pyloric valve
- cpv7n :
-
nerve innervating muscle cpv7
- cv :
-
muscles of the ventral cardiac ossicles
- cv1n :
-
nerve innervating muscle cvl
- cv2n :
-
nerve innervating muscle cv2
- EJP :
-
excitatory junctional potential
- IC :
-
inferior cardiac neuron
- IV :
-
inferior ventricular neuron
- IVN :
-
inferior ventricular nerve
- LP :
-
lateral pyloric neuron
- LPG :
-
lateral posterior gastric neuron
- lvn :
-
lateral ventricular nerve
- mvn :
-
medial ventricular nerve
- p :
-
muscles of the pylorus
- PD :
-
pyloric dilator neuron
- PD in :
-
intrinsic PD neuron
- PD ex :
-
extrinsic PD neuron
- pdn :
-
pyloric dilator nerve
- PY :
-
pyloric neuron
- pyn :
-
pyloric nerve
- STG :
-
stomatogastric ganglion
- VD :
-
ventricular dilator neuron
References
Beltz B, Eisen JS, Flamm R, Harris-Warrick RM, Hooper SL, Marder E (1984) Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Homarus americanus, Cancer irroratus, andPanulirus interruptus). J Exp Biol 109:35–54
Claiborne BJ, Selverston AI (1984) Localization of stomatogastric IV neuron cell bodies in lobster brain. J Comp Physiol A 154:27–32
Dando MR, Chanussot B, Nagy F (1974) Activation of command fibres to the stomatogastric ganglion by input from a gastric mill proprioceptor in the crab,Cancer pagurus. Mar Behav Physiol 2:197–228
Dickinson PS, Nagy F (1983) Control of a central pattern generator by an identified modulatory interneurone in Crustacea. II. Induction and modification of plateau properties in pyloric neurones. J Exp Biol 105:59–82
Eisen JS, Marder E (1982) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons. J Neurophysiol 48:1392–1415
Eisen JS, Marder E (1984) A mechanism for the production of phase shifts in a pattern generator. J Neurophysiol 51:1374–1393
Ghiselin MT (1966) An application of the theory of definitions to systematic principles. Syst Zool 15:127–130
Govind CK, Wiens TJ (1985) Innervation of the limb accessory flexor muscles in several decapod crustaceans. I. Anatomy. J Neurobiol 16:317–328
Govind CK, Atwood HL, Maynard DM (1975) Innervation and neuromuscular physiology of intrinsic foregut muscles in the blue crab and spiny lobster. J Comp Physiol 96:185–204
Harris-Warrick RM (1986) Chemical modulation of central pattern generators. In: Cohen AH, Rossignol S, Grillner S (eds) Neural control of rhythmic movements. John Wiley & Sons, New York, in press
Hartline DK, Gassie DV (1979) Pattern generation in the lobster (Panulirus) stomatogastric ganglion. I. Pyloric neuron kinetics and synaptic interactions. Biol Cybern 33:209–222
Hartline DK, Gassie DV, Sirchia CD (1979) Additions to the physiology of the stomatogastric ganglion (STG) of the spiny lobster. Soc Neurosci Abstr 5:248
Hartline DK, Gassie DV, Sirchia CD (1986) PY cell types in the stomatogastric ganglion ofPanulirus. In: Selverston AI, Moulins M (eds) The stomatogastric nervous system. Springer Berlin Heidelberg New York, (in press)
Hermann A (1979a) Generation of a fixed motor pattern. I. Details of synaptic interconnections of pyloric neurons in the stomatogastric ganglion of the crab,Cancer pagurus. J Comp Physiol 130:221–228
Hermann A (1979b) Generation of a fixed motor pattern. II. Electrical properties and synaptic characteristics of pyloric neurons in the stomatogastric ganglion of the crab,Cancer pagurus. J Comp Physiol 130:229–239
Hermann A, Dando MR (1977) Mechanisms of command fibre operation onto bursting pacemaker neurones in the stomatogastric ganglion of the crab,Cancer pagurus. J Comp Physiol 114:15–33
Hooper SL, Marder E (1984) Modulation of a central pattern generator by two neuropeptides, proctolin and FMRFamide. Brain Res 305:186–191
Kahan LB (1971) Neural control of postural muscles inCallianassa californiensis and three other species of decapod crustaceans. Comp Biochem Physiol 40 A: 1–18
LaMon BC, Miller JP (1985) Operation of the stomatogastric nervous systemin situ: modulation and function of pyloric motor patterns. Soc Neurosci Abstr 11:1022
Lingle CJ (1980) Sensitivity of decapod foregut muscles to acetylcholine and glutamate. J Comp Physiol 138:187–199
Marder E (1974) Acetylcholine as an excitatory neuromuscular transmitter in the stomatogastric system of the lobster. Nature 251:730–731
Marder E (1976) Cholinergic motor neurones in the stomatogastric system of the lobster. J Physiol 257:63–86
Marder E, Eisen JS (1984a) Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. J Neurophysiol 51:1345–1361
Marder E, Eisen JS (1984b) Electrically coupled pacemaker neurons respond differently to same physiological inputs and neurotransmitters. J Neurophysiol 51:1362–1373
Marder E, Hooper SL (1985) Neurotransmitter modulation of the stomatogastric ganglion of decapod crustaceans. In: Selverston AI (ed) Model networks and behavior. Plenum Publishing Co, New York, pp 319–337
Marder E, Paupardin-Tritsch D (1980) The pharmacological profile of acetylcholine response of a crustacean muscle. J Exp Biol 88:147–159
Maynard DM (1972) Simpler networks. Ann NY Acad Sci 193:59–72
Maynard DM, Dando MR (1974) The structure of the stomatogastric neuromuscular system inCallinectes sapidus, Homarus americanus, andPanulirus interruptus (Decapoda Crustacea). Philos Trans R Soc Lond B 268:161–220
Meiss DE, Norman RS (1977a) Comparative study of the stomatogastric system of several decapod crustacea. I. Skeleton. J Morphol 152:21–54
Meiss DE, Norman RS (1977b) Comparative study of the stomatogastric system of several decapod crustacea. II. Musculature. J Morphol 152:55–76
Meyrand P, Moulins M (1986) Myogenic oscillatory activity in the pyloric rhythmic motor system of Crustacea. J Comp Physiol A 158:489–503
Miller JP, Selverston AI (1982a) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. II. Oscillatory properties of pyloric neurons. J Neurophysiol 48:1378–1391
Miller JP, Selverston AI (1982b) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. IV. Network properties of pyloric system. J Neurophysiol 48:1416–1432
Mulloney B, Selverston AI (1974) Organization of the stomatogastric ganglion in the spiny lobster. I. Neurons driving the lateral teeth. J Comp Physiol 91:1–32
Nagy F, Dickinson PS (1983) Control of a central pattern generator by an identified interneurone in Crustacea. I. Modulation of the pyloric motor output. J Exp Biol 105: 33–58
O'Neil MB, Hooper SL, Wagner RJ, Marder E (1985) Homologous pyloric muscles are innervated by different motor neurons that release different neurotransmitters inPanulirus andCancer. Soc Neurosci Abstr 11:1021
Paul DH (1985a) Homologies between body movements and muscular contractions in the locomotion of two decapods of different families. J Exp Biol 94:159–168
Paul DH (1985b) Homologies between neuromuscular systems serving different functions in two decapods of different families. J Exp Biol 94:169–187
Paul DH, Alexander MT, Magnuson DA (1985) Evolution of the telson neuromusculature in decapod Crustacea. Biol Bull 168:106–124
Pearson KG, Boyan GS, Bastiani M, Goodman CS (1985) Heterogeneous properties of segmentally homologous interneurons in the ventral nerve cord of locusts. J Comp Neurol 233:133–145
Rezer E, Moulins M (1983) Expression of the crustacean pyloric pattern generator in the intact animal. J Comp Physiol 153:17–28
Robertson RM, Moulins M (1981) Oscillatory command input to the motor pattern generators of the crustacean stomatogastric ganglion. I. The pyloric rhythm. J Comp Physiol 143:453–463
Russell DF, Hartline DK (1978) Bursting neural networks: a reexamination. Science 200:453–456
Russell DF, Hartline DK (1982) Slow active potentials and bursting motor patterns in pyloric network of the lobster,Panulirus interruptus. J Neurophysiol 48:914–937
Schaefer N (1970) The functional morphology of the fore-gut of three species of decapod Crustacea:Cyclograpsus punctatus Milne-Edward,Diogenes brevirostris Stimpson, andUpogebia africana (Ortmann). Zoologica Africana 5:309–326
Schram SR (1982) The fossil record and evolution of Crustacea. In: Abele LG (ed) Systematics, the fossil record, and biogeography. (The biology of Crustacea, vol 1) Academic Press, New York, pp 93–147
Selverston AI, Miller JP (1980) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. I. Pyloric system. J Neurophysiol 44:1102–1121
Selverston AI, Moulins M (1985) Oscillatory neural networks. Annu Rev Physiol 47:29–48
Selverston AI, Russell DF, Miller JP, King DG (1976) The stomatogastric nervous system: structure and function of a small neural network. Prog Neurobiol 7:215–290
Sigvardt KA, Mulloney B (1982) Properties of synapses made by IVN command-interneurons in the stomatogastric ganglion of the spiny lobster,Panulirus interruptus. J Exp Biol 97:153–168
Wiens TJ, Govind CK (1985) Innervation of the limb accessory flexor muscle in several decapod crustaceans. II. Electrophysiology. J Neurobiol 16:349–359
Wiens TJ, Rathmayer W (1985) The distribution of the common inhibitory neuron in brachyuran limb musculature. J Comp Physiol A 156:305–313
Wilson JA, Hoyle G (1978) Serially homologous neurones as concomitants of functional specialization. Nature 274:377–379
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hooper, S.L., O'Neil, M.B., Wagner, R. et al. The innervation of the pyloric region of the crab,Cancer borealis: Homologous muscles in decapod species are differently innervated. J. Comp. Physiol. 159, 227–240 (1986). https://doi.org/10.1007/BF00612305
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00612305