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Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion

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Abstract

  1. 1.

    The neurons of the pyloric network of the lobster (Panulirus interruptus) stomatogastric ganglion organize their rhythmic motor output using both chemical and electrical synapses. The 6 electrical synapses within this network help set the firing phases of the pyloric neurons during each rhythmic cycle. We examined the modulatory effects of the amines dopamine (DA), serotonin (5HT) and octopamine (Oct) on coupling at all the electrical synapses of the pyloric network.

  2. 2.

    Electrical coupling within the pacemaker group [anterior burster (AB) to pyloric dilator (PD), and PD-

  3. 3.

    Dopamine decreased or increased the coupling strength of all the pyloric electrical synapses: the sign of the effect depended upon which neuron was the target of current injection. For example, DA decreased AB→ PD coupling (i.e., when current was injected into the AB) but increased coupling in the other direction, PD→ AB. Dopamine decreased AB to VD coupling when current was injected into either neuron. Serotonin also had mixed effects; it enhanced PD→AB coupling but decreased AB to VD and PD to VD coupling in both directions. Octopamine's only effect was to reduce PD→ VD coupling. li]4.

  4. 5.

    The characteristic modulation of electrical coupling by each amine may contribute to the unique motor pattern that DA, 5HT and Oct each elicit from the pyloric motor network.

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Abbreviations

AB:

anterior burster

CPG:

central pattern generator

DA:

dopamine

GSP:

graded synaptic potential

5HT:

serotonin

IC:

inferior cardiac

I/O:

input/output

LP:

lateral pyloric

Oct:

octopamine

PD:

pyloric dilator

PTX:

picrotoxin

PY:

pyloric constrictor

Rin :

input resistance

R1, R2 :

soma resistance

R1A, R2A :

axial resistance

R1D, R2D :

dendrite resistance

RJ :

junctional resistance

STG:

stomatogastric ganglion

TTX:

tetrodotoxin

VD:

ventral dilator

References

  • Anwyl R (1991) Modulation of vertebrate neuronal calcium channels by transmitters. Brain Res Rev 16:265–281

    Google Scholar 

  • Barker DL, Kushner PD, Hooper NK (1979) Synthesis of dopamine and octopamine in the crustacean stomatogastric nervous system. Brain Res 161:99–113

    Google Scholar 

  • Beltz B, Eisen J, Flamm R, Harris-Warrick RM, Hooper S, Marder E (1984) Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus and Cancer irroratus). J Exp Biol 109:35–54

    Google Scholar 

  • Bennett MVL (1977) Electrical transmission: a functional analysis and comparison to chemical transmission. In: Kandel ER (ed) Cellular biology of neurons, vol. 1, Sect. 1, Handbook of physiology, The nervous system. Williams and Wilkins, Baltimore, pp 357–416

    Google Scholar 

  • Berry MS, Cottrell GA (1979) Ionic basis of different synaptic potentials mediated by identified dopamine-containing neuron in Planorbis. Proc R Soc Lond B 203:417–444

    Google Scholar 

  • Berry MS, Pentreath VW (1977) The integrative properties of electrotonic synapses. Comp Biochem Physiol 57A: 289–295

    Google Scholar 

  • Bidaut M (1980) Pharmacological dissection of the pyloric network of the lobster stomatogastric ganglion using picrotoxin. J Neurophysiol 44:1089–1101

    Google Scholar 

  • Carew TJ, Kandel ER (1976) Two functional effects of decreased conductance EPSPs: synaptic augmentation and increased electrotonic coupling. Science 192:150–153

    Google Scholar 

  • Colombaioni L, Brunelli M (1988) Neurotransmitter-induced modulation of an electrotonic synapse in the CNS of Hirudo medicinalis. Exp Biol 47:139–144

    Google Scholar 

  • Dowling JE (1991) Retinal neuromodulation: the role of dopamine. Visual Neurosci 7:87–97

    Google Scholar 

  • Edwards DH, Heitler WJ, Leise EM, Fricke RA (1991) Postsynaptic modulation of rectifying electrical synaptic inputs to the LG escape command neuron in crayfish. J Neurosci 11:2117–2129

    Google Scholar 

  • 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

    Google Scholar 

  • Flamm RE, Harris-Warrick RM (1986a) Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. J Neurophysiol 55:847–865

    Google Scholar 

  • Flamm RE, Harris-Warrick RM (1986b) Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine and serotonin within the pyloric circuit. J Neurophysiol 55:866–881

    Google Scholar 

  • Friesen WO (1985) Neuronal control of leech swimming movements: interactions between cell 60 and previously described oscillator neurons. J Comp Physiol A 156:231–242

    Google Scholar 

  • Furshpan EJ, Potter DD (1959) Transmission at the giant motor synapses of the crayfish. J Physiol (Lond) 145:289–325

    Google Scholar 

  • Getting P (1988) Comparative analysis of invertebrate central pattern generators. In: Cohen AH, Rosignol S, Grillner S (eds) Neural control of rhythmic movements. John Wiley, New York, pp 101–128

    Google Scholar 

  • Giaume C, Kado RT, Korn H (1987) Voltage-clamp analysis of a crayfish rectifying synapse. J Physiol (Lond) 386:91–112

    Google Scholar 

  • Gola M, Selverston AI (1981) Ionic requirements for bursting activity in lobster stomatogastric neurons. J Comp Physiol 145:191–207

    Google Scholar 

  • Graubard K, Hartline DK (1987) Full wave rectification from a mixed electrical-chemical synapse. Science 237:535–537

    Google Scholar 

  • Hall DH, Marder E, Bennett MVL (1985) Interneuronal and interglial gap junctions in the stomatogastric ganglion of the rock crab. Neurosci Abstr 11:506

    Google Scholar 

  • Hampson ECGM, Vaney DI, Weiler R (1992) Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J Neurosci 12:4911–4922

    Google Scholar 

  • Harris-Warrick RM (1988) Chemical modulation of central pattern generators. In: Cohen AH, Rosignol S, Grillner S (eds) Neural control of rhythmic movements. John Wiley, New York, pp 285–331

    Google Scholar 

  • Harris-Warrick RM, Flamm RE (1987) Multiple mechanisms of bursting in a conditional burster neuron. J Neurosci 7:2113–2128

    Google Scholar 

  • Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14:39–57

    Article  CAS  PubMed  Google Scholar 

  • Harris-Warrick RM, Nagy F, Nusbaum MP (1992) Neuromodulation of stomatogastric networks by identified neurons and transmitters. In: Harris-Warrick RM, Marder E, Selverston AI, Moulins M (eds) Dynamic biological networks: the stomatogastric nervous system. MIT Press, Cambridge, pp 87–137

    Google Scholar 

  • Hartline DK, Graubard K (1992) Cellular and synaptic properties in the crustacean stomatogastric nervous system. In: HarrisWarrick RM, Marder E, Selverston AI, Moulins M (eds) Dynamic biological networks: the stomatogastric nervous system. MIT Press, Cambridge, pp 31–85

    Google Scholar 

  • Hartline DK, Gassie DV, Sirchia CD (1987) PY cell types in the stomatogastric ganglion of Panulirus. In: Selverston AI, Moulins M (eds) The crustacean stomatogastric system. Springer, Berlin Heidelberg New York, pp 75–77

    Google Scholar 

  • Hartline DK, Russell DF, Raper JA, Graubard K (1988) Special cellular and synaptic mechanisms in motor pattern generation. Comp Biochem Physiol 91C: 115–131

    Google Scholar 

  • Heitler WJ, Fraser K, Edwards DH (1991) Different types of rectification at electrical synapses made by a single crayfish neurone investigated experimentally and by computer simulation. J Comp Physiol A 169:707–718

    Google Scholar 

  • Hermann A (1979) Generation of a fixed motor pattern I. Details of synaptic interactions of pyloric neurons in the stomatogastric ganglion of the crab, Cancer pagurus. J Comp Physiol 130:221–228

    Google Scholar 

  • Hooper SL, Marder E (1987) Modulation of a central pattern generator by the peptide, proctolin. J Neurosci 7:2097–2112

    Google Scholar 

  • Johnson BR, Harris-Warrick RM (1990) Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion. J Neurosci 10:2066–2076

    Google Scholar 

  • Johnson BR, Hooper SL (1992) Overview of the stomatogastric nervous system. In: Harris-Warrick RM, Marder E, Selverston AI, Moulins M (eds) Dynamic biological networks: the stomatogastric nervous system. MIT Press, Cambridge, pp 1–30

    Google Scholar 

  • Johnson BR, Peck JH, Harris-Warrick RM (1991) Temperature sensitivity of graded synaptic transmission in the lobster stomatogastric ganglion. J Exp Biol 156:267–285

    Google Scholar 

  • Johnson BR, Peck JH, Harris-Warrick RM (1992a) Amine modulation of mixed chemical-electrical synapses in the pyloric network of the lobster stomatogastric ganglion. Neurosci Abstr 18:1055

    Google Scholar 

  • Johnson BR, Peck JH, Harris-Warrick RM (1992b) Elevated temperature alters the ionic dependence of amine-induced pacemaker activity in a conditional burster neuron. J Comp Physiol A 170:201–209

    Google Scholar 

  • Katz PS, Eigg MH, Harris-Warrick RM (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system: I. Identification and characterization of the gastro-pyloric receptor cells. J Neurophysiol 62:558–570

    Google Scholar 

  • Kravitz EA (1988) Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 241:1775–1781

    Google Scholar 

  • Marder E (1984) Roles for electrical coupling in neural circuits as revealed by selective neuronal deletions. J Exp Biol 112:147–167

    Google Scholar 

  • Marder E, Eisen JS (1984) Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. J Neurophysiol 51:1345–1361

    Google Scholar 

  • Miller JP (1980) Mechanisms underlying pattern generation in the lobster stomatogastric ganglion. PhD thesis, University of California, San Diego, CA

    Google Scholar 

  • Miller JP (1987) Pyloric mechanisms. In: Selverston AI, Moulins M (eds) The crustacean stomatogastric system. Springer, Berlin Heidelberg New York, pp 109–136

    Google Scholar 

  • Miller JP, Selverston AI (1979) Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 206:702–704

    CAS  PubMed  Google Scholar 

  • Mulloney B (1987) Neural circuits. In: Selverston AI, Moulins M (eds) The crustacean stomatogastric system. Springer, Berlin Heidelberg New York, pp 57–77

    Google Scholar 

  • Mulloney B, Selverston AI (1974) Organization of the stomatogastric ganglion of the spiny lobster. I. Neurons driving the lateral teeth. J Comp Physiol 91:1–32

    Google Scholar 

  • Nagy F, Miller JP (1987) Pyloric pattern generation in Panulirus interruptus is terminated by blockade of activity through the stomatogastric nerve. In: Selverston AI, Moulins M (eds) The crustacean stomatogastric system. Springer, Berlin Heidelberg New York, pp 136–139

    Google Scholar 

  • Ramon F, Rivera A (1986) Gap junction channel modulation a physiological viewpoint. Prog Biophys Molec Biol 48:127–153

    Google Scholar 

  • Raper JA (1979) Non-impulse mediated synaptic transmission in the stomatogastric ganglion of the spiny lobster. PhD thesis, University of California, San Diego, CA

    Google Scholar 

  • Russell DF (1979) CNS control of pattern generation in the lobster stomatogastric ganglion. Brain Res 177:598–602

    Google Scholar 

  • Selverston AI (1987) Gastric mill mechanisms. In: Selverston AI, Moulins M (eds) The crustacean stomatogastric system. Springer, Berlin Heidelberg New York, pp 147–171

    Google Scholar 

  • Selverston AI, Russell DF, Miller JP, King DG (1976) The stomatogastric nervous system: structure and function of a small neural network. Prog Neurobiol 7:215–289

    Google Scholar 

  • Spira ME, Spray DC, Bennett MVL (1980) Synaptic organization of expansion motoneurons of Navanax inermis. Brain Res 195:241–269

    Google Scholar 

  • Spray DC, Bennett MVL (1985) Physiology and pharmacology of gap junctions. Annu Rev Physiol 47:281–303

    Google Scholar 

  • Spray DC, White RL, Verselis V, Bennett MVL (1985) General and comparative physiology of gap junction channels. In: Bennett MVL, Spray DC (eds) Gap junctions. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 139–153

    Google Scholar 

  • Zipser B (1979) Voltage-modulated membrane resistance in coupled leech neurons. J Neurophysiol 42:465–475

    Google Scholar 

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Johnson, B.R., Peck, J.H. & Harris-Warrick, R.M. Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion. J Comp Physiol A 172, 715–732 (1993). https://doi.org/10.1007/BF00195397

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