Skip to main content
SpringerLink
Log in

Modulation of stomatogastric rhythms

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Neuromodulation by peptides and amines is a primary source of plasticity in the nervous system as it adapts the animal to an ever-changing environment. The crustacean stomatogastric nervous system is one of the premier systems to study neuromodulation and its effects on motor pattern generation at the cellular level. It contains the extensively modulated central pattern generators that drive the gastric mill (chewing) and pyloric (food filtering) rhythms. Neuromodulators affect all stages of neuronal processing in this system, from membrane currents and synaptic transmission in network neurons to the properties of the effector muscles. The ease with which distinct neurons are identified and their activity is recorded in this system has provided considerable insight into the mechanisms by which neuromodulators affect their target cells and modulatory neuron function. Recent evidence suggests that neuromodulators are involved in homeostatic processes and that the modulatory system itself is under modulatory control, a fascinating topic whose surface has been barely scratched. Future challenges include exploring the behavioral conditions under which these systems are activated and how their effects are regulated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AB:

Anterior burster

CoG:

Commissural ganglion

CPG:

Central pattern generator

CPN2:

Commissural projection neuron 2

GABA:

γ-Aminobutyric acid

GM:

Gastric mill neurons

GPR:

Gastro-pyloric receptor

I A :

A-type current

Ih :

h-type current

I HTK :

High-threshold potassium current

I MIC :

Neuromodulator-induced current

LG:

Lateral gastric neuron

LP:

Lateral pyloric neuron

MCN:

Modulatory commissural neuron

MPN:

Modulatory proctolin neuron

PD:

Pyloric dilator neuron

STG:

Stomatogastric ganglion

STNS:

Stomatogastric nervous system

References

  • Arshavsky YI, Orlovsky GN, Perret C (1988) Activity of rubrospinal neurons during locomotion and scratching in the cat. Behav Brain Res 28:193–199

    Article  CAS  PubMed  Google Scholar 

  • Atwood HL (1976) Organization and synaptic physiology of crustacean neuromuscular systems. Prog Neurobiol 7:291–391

    Article  CAS  PubMed  Google Scholar 

  • Atwood HL, Wiersma CA (1967) Command interneurons in the crayfish central nervous system. J Exp Biol 46:249–261

    CAS  PubMed  Google Scholar 

  • Atwood HL, Wojtowicz JM (1986) Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. Int Rev Neurobiol 28:275–362

    Article  CAS  PubMed  Google Scholar 

  • Ayali A, Harris-Warrick RM (1999) Monoamine control of the pacemaker kernel and cycle frequency in the lobster pyloric network. J Neurosci 19:6712–6722

    CAS  PubMed  Google Scholar 

  • Ayali A, Johnson BR, Harris-Warrick RM (1998) Dopamine modulates graded and spike-evoked synaptic inhibition independently at single synapses in pyloric network of lobster. J Neurophysiol 79:2063–2069

    CAS  PubMed  Google Scholar 

  • Ballo AW, Bucher D (2009) Complex intrinsic membrane properties and dopamine shape spiking activity in a motor axon. J Neurosci 29:5062–5074

    Article  CAS  PubMed  Google Scholar 

  • Bässler U, Büschges A (1998) Pattern generation for stick insect walking movements—multisensory control of a locomotor program. Brain Res Rev 27:65–88

    Article  PubMed  Google Scholar 

  • Beenhakker MP, Blitz DM, Nusbaum MP (2004) Long-lasting activation of rhythmic neuronal activity by a novel mechanosensory system in the crustacean stomatogastric nervous system. J Neurophysiol 91:78–91

    Article  PubMed  Google Scholar 

  • Beenhakker MP, DeLong ND, Saideman SR, Nadim F, Nusbaum MP (2005) Proprioceptor regulation of motor circuit activity by presynaptic inhibition of a modulatory projection neuron. J Neurosci 25:8794–8806

    Article  CAS  PubMed  Google Scholar 

  • Beenhakker MP, Kirby MS, Nusbaum MP (2007) Mechanosensory gating of proprioceptor input to modulatory projection neurons. J Neurosci 27:14308–14316

    Article  CAS  PubMed  Google Scholar 

  • Billimoria CP, Li L, Marder E (2005) Profiling of neuropeptides released at the stomatogastric ganglion of the crab, Cancer borealis with mass spectrometry. J Neurochem 95:191–199

    Article  CAS  PubMed  Google Scholar 

  • Billimoria CP, DiCaprio RA, Birmingham JT, Abbott LF, Marder E (2006) Neuromodulation of spike-timing precision in sensory neurons. J Neurosci 26:5910–5919

    Article  CAS  PubMed  Google Scholar 

  • Birmingham JT (2001) Increasing sensor flexibility through neuromodulation. Biol Bull 200:206–210

    Article  CAS  PubMed  Google Scholar 

  • Birmingham JT, Tauck DL (2003) Neuromodulation in invertebrate sensory systems: from biophysics to behavior. J Exp Biol 206:3541–3546

    Article  PubMed  Google Scholar 

  • Birmingham JT, Szuts ZB, Abbott LF, Marder E (1999) Encoding of muscle movement on two time scales by a sensory neuron that switches between spiking and bursting modes. J Neurophysiol 82:2786–2797

    CAS  PubMed  Google Scholar 

  • Birmingham JT, Billimoria CP, DeKlotz TR, Stewart RA, Marder E (2003) Differential and history-dependent modulation of a stretch receptor in the stomatogastric system of the crab, Cancer borealis. J Neurophysiol 90:3608–3616

    Article  CAS  PubMed  Google Scholar 

  • Blitz DM, Nusbaum MP (1997) Motor pattern selection via inhibition of parallel pathways. J Neurosci 17:4965–4975

    CAS  PubMed  Google Scholar 

  • Blitz DM, Nusbaum MP (1999) Distinct functions for cotransmitters mediating motor pattern selection. J Neurosci 19:6774–6783

    CAS  PubMed  Google Scholar 

  • Blitz DM, Nusbaum MP (2008) State-dependent presynaptic inhibition regulates central pattern generator feedback to descending inputs. J Neurosci 28:9564–9574

    Article  CAS  PubMed  Google Scholar 

  • Blitz DM, Christie AE, Coleman MJ, Norris BJ, Marder E, Nusbaum MP (1999) Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network. J Neurosci 19:5449–5463

    CAS  PubMed  Google Scholar 

  • Blitz DM, Beenhakker MP, Nusbaum MP (2004) Different sensory systems share projection neurons but elicit distinct motor patterns. J Neurosci 24:11381–11390

    Article  CAS  PubMed  Google Scholar 

  • Blitz DM, White RS, Saideman SR, Cook A, Christie AE, Nadim F, Nusbaum MP (2008) A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons. J Exp Biol 211:1000–1011

    Article  PubMed  Google Scholar 

  • Bowerman RF, Larimer JL (1974a) Command fibres in the circumoesophogeal connectives of crayfish. I. Tonic fibres. J Exp Biol 60:95–117

    Google Scholar 

  • Bowerman RF, Larimer JL (1974b) Command fibres in the circumoesophogeal connectives of crayfish. II. Phasic fibres. J Exp Biol 60:119–134

    Google Scholar 

  • Branchereau P, Chapron J, Meyrand P (2002) Descending 5-hydroxytryptamine raphe inputs repress the expression of serotonergic neurons and slow the maturation of inhibitory systems in mouse embryonic spinal cord. J Neurosci 22:2598–2606

    CAS  PubMed  Google Scholar 

  • Buchanan JT, Einum JF (2008) The spinobulbar system in lamprey. Brain Res Rev 57:37–45

    Article  PubMed  Google Scholar 

  • Bucher D, Thirumalai V, Marder E (2003) Axonal dopamine receptors activate peripheral spike initiation in a stomatogastric motor neuron. J Neurosci 23:6866–6875

    CAS  PubMed  Google Scholar 

  • Bucher D, Prinz AA, Marder E (2005) Animal-to-animal variability in motor pattern production in adults and during growth. J Neurosci 25:1611–1619

    Article  CAS  PubMed  Google Scholar 

  • Burnstock G (2004) Cotransmission. Curr Opin Pharmacol 4:47–52

    Article  CAS  PubMed  Google Scholar 

  • Büschges A, Ludwar BC, Bucher D, Schmidt J, DiCaprio RA (2004) Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system. Eur J Neurosci 19:1856–1862

    Article  PubMed  Google Scholar 

  • Cantrell AR, Catterall WA (2001) Neuromodulation of Na+ channels: an unexpected form of cellular plasticity. Nat Rev Neurosci 2:397–407

    Article  CAS  PubMed  Google Scholar 

  • Cape SS, Rehm KJ, Ma M, Marder E, Li L (2008) Mass spectral comparison of the neuropeptide complement of the stomatogastric ganglion and brain in the adult and embryonic lobster, Homarus americanus. J Neurochem 105:690–702

    Article  CAS  PubMed  Google Scholar 

  • Cazalets JR, Nagy F, Moulins M (1987) Suppressive control of a rhythmic central pattern generator by an identified modulatory neuron in crustacea. Neurosci Lett 81:267–272

    Article  CAS  PubMed  Google Scholar 

  • Cazalets JR, Nagy F, Moulins M (1990a) Suppressive control of the crustacean pyloric network by a pair of identified interneurons. I. Modulation of the motor pattern. J Neurosci 10:448–457

    CAS  PubMed  Google Scholar 

  • Cazalets JR, Nagy F, Moulins M (1990b) Suppressive control of the crustacean pyloric network by a pair of identified interneurons. II. Modulation of neuronal properties. J Neurosci 10:458–468

    CAS  PubMed  Google Scholar 

  • Chen R, Ma M, Hui L, Zhang J, Li L (2009) Measurement of neuropeptides in crustacean hemolymph via MALDI mass spectrometry. J Am Soc Mass Spectrom 20:708–718

    Article  CAS  PubMed  Google Scholar 

  • Christie AE, Skiebe P, Marder E (1995) Matrix of neuromodulators in neurosecretory structures of the crab Cancer borealis. J Exp Biol 198:2431–2439

    CAS  PubMed  Google Scholar 

  • Christie AE, Lundquist CT, Nassel DR, Nusbaum MP (1997) Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis. J Exp Biol 200:2279–2294

    CAS  PubMed  Google Scholar 

  • Christie AE, Stein W, Quinlan JE, Beenhakker MP, Marder E, Nusbaum MP (2004) Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab Cancer borealis. J Comp Neurol 469:153–169

    Article  CAS  PubMed  Google Scholar 

  • Christie AE, Stemmler EA, Peguero B, Messinger DI, Provencher HL, Scheerlinck P, Hsu YW, Guiney ME, de la Iglesia HO, Dickinson PS (2006) Identification, physiological actions, and distribution of VYRKPPFNGSIFamide (Val1)-SIFamide) in the stomatogastric nervous system of the American lobster Homarus americanus. J Comp Neurol 496:406–421

    Article  CAS  PubMed  Google Scholar 

  • Claiborne BJ, Selverston AI (1984a) Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster. J Neurosci 4:708–721

    CAS  PubMed  Google Scholar 

  • Claiborne BJ, Selverston AI (1984b) Localization of stomatogastric IV neuron cell bodies in lobster brain. J Comp Physiol A 154:27–32

    Article  Google Scholar 

  • Claiborne BJ, Selverston AI (1987) Functional anatomy and behavior. The crustacean stomatogastric system—a model for the study of central nervous systems. Springer, Berlin, pp 9–27

    Google Scholar 

  • Clark MC, Dever TE, Dever JJ, Xu P, Rehder V, Sosa MA, Baro DJ (2004) Arthropod 5-HT2 receptors: a neurohormonal receptor in decapod crustaceans that displays agonist independent activity resulting from an evolutionary alteration to the DRY motif. J Neurosci 24:3421–3435

    Article  CAS  PubMed  Google Scholar 

  • Coleman MJ, Nusbaum MP (1994) Functional consequences of compartmentalization of synaptic input. J Neurosci 14:6544–6552

    CAS  PubMed  Google Scholar 

  • Coleman MJ, Nusbaum MP, Cournil I, Claiborne BJ (1992) Distribution of modulatory inputs to the stomatogastric ganglion of the crab, Cancer borealis. J Comp Neurol 325:581–594

    Article  CAS  PubMed  Google Scholar 

  • Coleman MJ, Meyrand P, Nusbaum MP (1995) A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378:502–505

    Article  CAS  PubMed  Google Scholar 

  • Combes D, Simmers J, Moulins M (1997) Conditional dendritic oscillators in a lobster mechanoreceptor neurone. J Physiol 499(Pt 1):161–177

    CAS  PubMed  Google Scholar 

  • Combes D, Meyrand P, Simmers J (1999) Motor pattern specification by dual descending pathways to a lobster rhythm-generating network. J Neurosci 19:3610–3619

    CAS  PubMed  Google Scholar 

  • Cymbalyuk GS, Quentin G, Masino MA, Calabrese RL (2002) Bursting in leech heart interneurons: cell-autonomous and network-based mechanisms. J Neurosci 22:10580–10592

    CAS  PubMed  Google Scholar 

  • Dagher A, Robbins TW (2009) Personality, addiction, dopamine: insights from Parkinson’s disease. Neuron 61:502–510

    Article  CAS  PubMed  Google Scholar 

  • Dando MR, Selverston AI (1972) Command fibres from the supra-oesophageal ganglion to the stomatogastric ganglion in Panulirus argus. J Comp Physiol A 78:138–175

    Article  Google Scholar 

  • Daur N, Nadim F, Stein W (2009) Regulation of motor patterns by the central spike-initiation zone of a sensory neuron. Eur J Neurosci 30:808–822

    Article  PubMed  Google Scholar 

  • Davis GW (2006) Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 29:307–323

    Article  CAS  PubMed  Google Scholar 

  • DeLorme EM, Rabe CS, McGee R Jr (1988) Regulation of the number of functional voltage-sensitive Ca++ channels on PC12 cells by chronic changes in membrane potential. J Pharmacol Exp Ther 244:838–843

    CAS  PubMed  Google Scholar 

  • Desai NS, Rutherford LC, Turrigiano GG (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2:515–520

    Article  CAS  PubMed  Google Scholar 

  • Dickinson PS (2006) Neuromodulation of central pattern generators in invertebrates and vertebrates. Curr Opin Neurobiol 16:604–614

    Article  CAS  PubMed  Google Scholar 

  • Dickinson PS, Mecsas C, Marder E (1990) Neuropeptide fusion of two motor-pattern generator circuits. Nature 344:155–158

    Article  CAS  PubMed  Google Scholar 

  • Dubuc R, Grillner S (1989) The role of spinal cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey. Brain Res 483:196–200

    Article  CAS  PubMed  Google Scholar 

  • Dudel J, Kuffler SW (1961) Mechanism of facilitation at the crayfish neuromuscular junction. J Physiol 155:530–542

    CAS  PubMed  Google Scholar 

  • Edwards DH, Heitler WJ, Krasne FB (1999) Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci 22:153–161

    Article  CAS  PubMed  Google Scholar 

  • Ezure K, Tanaka I (1997) Convergence of central respiratory and locomotor rhythms onto single neurons of the lateral reticular nucleus. Exp Brain Res 113:230–242

    Article  CAS  PubMed  Google Scholar 

  • Faumont S, Combes D, Meyrand P, Simmers J (2005) Reconfiguration of multiple motor networks by short- and long-term actions of an identified modulatory neuron. Eur J Neurosci 22:2489–2502

    Article  PubMed  Google Scholar 

  • Fenelon VS, Kilman V, Meyrand P, Marder E (1999) Sequential developmental acquisition of neuromodulatory inputs to a central pattern-generating network. J Comp Neurol 408:335–351

    Article  CAS  PubMed  Google Scholar 

  • Fénelon VS, Le Feuvre Y, Meyrand P (2002) Role of modulatory inputs in the ontogeny of neural networks. Springer-Verlag, New York, LLC

    Google Scholar 

  • Fleischer AG (1981) The effect of eyestalk hormones on the gastric mill in the intact lobster, Panulirus interruptus. J Comp Physiol A 141:363–368

    Article  Google Scholar 

  • Frost WN, Katz PS (1996) Single neuron control over a complex motor program. Proc Natl Acad Sci USA 93:422–426

    Article  CAS  PubMed  Google Scholar 

  • Galante M, Avossa D, Rosato-Siri M, Ballerini L (2001) Homeostatic plasticity induced by chronic block of AMPA/kainate receptors modulates the generation of rhythmic bursting in rat spinal cord organotypic cultures. Eur J Neurosci 14:903–917

    Article  CAS  PubMed  Google Scholar 

  • Gansert J, Golowasch J, Nadim F (2007) Sustained rhythmic activity in gap-junctionally coupled networks of model neurons depends on the diameter of coupled dendrites. J Neurophysiol 98:3450–3460

    Article  PubMed  Google Scholar 

  • Gillette R, Kovac MP, Davis WJ (1978) Command neurons in Pleurobranchaea receive synaptic feedback from the motor network they excite. Science 199:798–801

    Article  CAS  PubMed  Google Scholar 

  • Goaillard JM, Schulz DJ, Kilman VL, Marder E (2004) Octopamine modulates the axons of modulatory projection neurons. J Neurosci 24:7063–7073

    Article  CAS  PubMed  Google Scholar 

  • Golowasch J, Abbott LF, Marder E (1999a) Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J Neurosci 19:1–5

    Google Scholar 

  • Golowasch J, Casey M, Abbott LF, Marder E (1999b) Network stability from activity-dependent regulation of neuronal conductances. Neural Comput 11:1079–1096

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Islas C, Wenner P (2006) Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 49:563–575

    Article  CAS  PubMed  Google Scholar 

  • Graubard K, Raper JA, Hartline DK (1980) Graded synaptic transmission between spiking neurons. Proc Natl Acad Sci USA 77:3733–3735

    Article  CAS  PubMed  Google Scholar 

  • Graubard K, Raper JA, Hartline DK (1983) Graded synaptic transmission between identified spiking neurons. J Neurophysiol 50:508–521

    CAS  PubMed  Google Scholar 

  • Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815–835

    Article  CAS  PubMed  Google Scholar 

  • Haedo RJ, Golowasch J (2006) Ionic mechanism underlying recovery of rhythmic activity in adult isolated neurons. J Neurophysiol 96:1860–1876

    Article  CAS  PubMed  Google Scholar 

  • Harris-Warrick RM, Marder E, Selverston AI, Moulins M (1992) Dynamic biological networks: the stomatogastric nervous system. MIT Press, Cambridge

    Google Scholar 

  • Harris-Warrick RM, Johnson BR, Peck JH, Kloppenburg P, Ayali A, Skarbinski J (1998) Distributed effects of dopamine modulation in the crustacean pyloric network. Ann N Y Acad Sci 860:155–167

    Article  CAS  PubMed  Google Scholar 

  • Hartline DK, Graubard K (1992) Cellular and synaptic properties in the crustacean stomatogastric nervous system. Dynamic biological networks: the stomatogastric nervous system. MIT Press, Cambridge, pp 31–86

    Google Scholar 

  • Hartline DK, Maynard DM (1975) Motor patterns in the stomatogastric ganglion of the lobster Panulirus argus. J Exp Biol 62:405–420

    CAS  PubMed  Google Scholar 

  • Hedrich UB, Stein W (2008) Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system. J Exp Biol 211:2624–2637

    Article  PubMed  Google Scholar 

  • Hedrich UB, Smarandache CR, Stein W (2009) Differential activation of projection neurons by two sensory pathways contributes to motor pattern selection. J Neurophysiol (epub ahead of print)

  • Heinzel HG, Weimann JM, Marder E (1993) The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic and electrophysiological examination. J Neurosci 13:1793–1803

    CAS  PubMed  Google Scholar 

  • Hempel CM, Vincent P, Adams SR, Tsien RY, Selverston AI (1996) Spatio-temporal dynamics of cyclic AMP signals in an intact neural circuit. Nature 384:166–169

    Article  CAS  PubMed  Google Scholar 

  • Hong SJ, Lnenicka GA (1995) Activity-dependent reduction in voltage-dependent calcium current in a crayfish motoneuron. J Neurosci 15:3539–3547

    CAS  PubMed  Google Scholar 

  • Hooper SL (2003) Crustacean stomatogastric system. In: Arbib MA (ed) The handbook of brain theory and neural networks. MIT Press, Cambridge, pp 304–308

    Google Scholar 

  • Hooper SL, DiCaprio RA (2004) Crustacean motor pattern generator networks. NeuroSignals 13:50–69

    Article  CAS  PubMed  Google Scholar 

  • Hooper SL, O’Neil MB, Wagner R, Ewer J, Golowasch J, Marder E (1986) The innervation of the pyloric region of the crab, Cancer borealis: homologous muscles in decapod species are differently innervated. J Comp Physiol A 159:227–240

    Article  CAS  PubMed  Google Scholar 

  • Jan LY, Jan YN (1982) Peptidergic transmission in sympathetic ganglia of the frog. J Physiol 327:219–246

    CAS  PubMed  Google Scholar 

  • Johnson BR, Peck JH, Harris-Warrick RM (1993) Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion. J Comp Physiol A 172:715–732

    Article  CAS  PubMed  Google Scholar 

  • Johnson BR, Peck JH, Harris-Warrick RM (1994) Differential modulation of chemical and electrical components of mixed synapses in the lobster stomatogastric ganglion. J Comp Physiol A 175:233–249

    Article  CAS  PubMed  Google Scholar 

  • Jorge-Rivera JC, Marder E (1996) TNRNFLRFamide and SDRNFLRFamide modulate muscles of the stomatogastric system of the crab Cancer borealis. J Comp Physiol A 179:741–751

    Article  CAS  PubMed  Google Scholar 

  • Jorge-Rivera J, Marder YE (1997) Allatostatin decreases stomatogastric neuromuscular transmission in the crab Cancer borealis. J Exp Biol 200:2937–2946

    CAS  PubMed  Google Scholar 

  • Jorge-Rivera JC, Sen K, Birmingham JT, Abbott LF, Marder E (1998) Temporal dynamics of convergent modulation at a crustacean neuromuscular junction. J Neurophysiol 80:2559–2570

    CAS  PubMed  Google Scholar 

  • Kaczmarek LK, Levitan IB (1987) Neuromodulation: the biochemical control of neuronal excitability. Oxford University Press, USA

    Google Scholar 

  • Katz PS (1998) Comparison of extrinsic and intrinsic neuromodulation in two central pattern generator circuits in invertebrates. Exp Physiol 83:281–292

    CAS  PubMed  Google Scholar 

  • Katz PS, Frost WN (1996) Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19:54–61

    Article  CAS  PubMed  Google Scholar 

  • Katz PS, Harris-Warrick RM (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. J Neurophysiol 62:571–581

    CAS  PubMed  Google Scholar 

  • Katz PS, Harris-Warrick RM (1990) Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents. J Neurosci 10:1495–1512

    CAS  PubMed  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 gastropyloric receptor cells. J Neurophysiol 62:558–570

    CAS  PubMed  Google Scholar 

  • Katz PS, Kirk MD, Govind CK (1993) Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release. J Neurosci 13:3075–3089

    CAS  PubMed  Google Scholar 

  • Khorkova O, Golowasch J (2007) Neuromodulators, not activity, control coordinated expression of ionic currents. J Neurosci 27:8709–8718

    Article  CAS  PubMed  Google Scholar 

  • Kiehn O, Harris-Warrick RM (1992a) 5-HT modulation of hyperpolarization-activated inward current and calcium-dependent outward current in a crustacean motor neuron. J Neurophysiol 68:496–508

    CAS  PubMed  Google Scholar 

  • Kiehn O, Harris-Warrick RM (1992b) Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual-conductance mechanism. J Neurophysiol 68:485–495

    CAS  PubMed  Google Scholar 

  • Kilman V, Fenelon VS, Richards KS, Thirumalai V, Meyrand P, Marder E (1999) Sequential developmental acquisition of cotransmitters in identified sensory neurons of the stomatogastric nervous system of the lobsters, Homarus americanus and Homarus gammarus. J Comp Neurol 408:318–334

    Article  CAS  PubMed  Google Scholar 

  • Kirby MS, Nusbaum MP (2007) Central nervous system projections to and from the commissural ganglion of the crab Cancer borealis. Cell Tissue Res 328:625–637

    Article  PubMed  Google Scholar 

  • Knable MB, Weinberger DR (1997) Dopamine, the prefrontal cortex and schizophrenia. J Psychopharmacol 11:123–131

    Article  CAS  PubMed  Google Scholar 

  • Krichmar JL (2008) The neuromodulatory system: a framework for survival and adaptive behavior in a challenging world. Adapt Behav 16:385–399

    Article  Google Scholar 

  • Kristan WB Jr, Calabrese RL, Friesen WO (2005) Neuronal control of leech behavior. Prog Neurobiol 76:279–327

    Article  PubMed  Google Scholar 

  • Kupfermann I (1979) Modulatory actions of neurotransmitters. Annu Rev Neurosci 2:447–465

    Article  CAS  PubMed  Google Scholar 

  • Kupfermann I, Weiss KR (1978) The command neuron concept. Behav Brain Sci 1:3–39

    Article  Google Scholar 

  • Le T, Verley DR, Goaillard JM, Messinger DI, Christie AE, Birmingham JT (2006) Bistable behavior originating in the axon of a crustacean motor neuron. J Neurophysiol 95:1356–1368

    Article  PubMed  Google Scholar 

  • Li L, Pulver SR, Kelley WP, Thirumalai V, Sweedler JV, Marder E (2002) Orcokinin peptides in developing and adult crustacean stomatogastric nervous systems and pericardial organs. J Comp Neurol 444:227–244

    Article  CAS  PubMed  Google Scholar 

  • Li L, Kelley WP, Billimoria CP, Christie AE, Pulver SR, Sweedler JV, Marder E (2003) Mass spectrometric investigation of the neuropeptide complement and release in the pericardial organs of the crab, Cancer borealis. J Neurochem 87:642–656

    Article  CAS  PubMed  Google Scholar 

  • Lingle C (1980) The sensitivity of decapod foregut muscles to acetylcholine and glutamate. J Comp Physiol A 138:187–199

    Article  CAS  Google Scholar 

  • Linsdell P, Moody WJ (1994) Na+ channel mis-expression accelerates K+ channel development in embryonic Xenopus laevis skeletal muscle. J Physiol 480(Pt 3):405–410

    CAS  PubMed  Google Scholar 

  • Liu Z, Golowasch J, Marder E, Abbott LF (1998) A model neuron with activity-dependent conductances regulated by multiple calcium sensors. J Neurosci 18:2309–2320

    CAS  PubMed  Google Scholar 

  • Lopez HS, Brown AM (1992) Neuromodulation. Curr Opin Neurobiol 2:317–322

    Article  CAS  PubMed  Google Scholar 

  • Luther JA, Robie AA, Yarotsky J, Reina C, Marder E, Golowasch J (2003) Episodic bouts of activity accompany recovery of rhythmic output by a neuromodulator- and activity-deprived adult neural network. J Neurophysiol 90:2720–2730

    Article  PubMed  Google Scholar 

  • MacLean JN, Zhang Y, Johnson BR, Harris-Warrick RM (2003) Activity-independent homeostasis in rhythmically active neurons. Neuron 37:109–120

    Article  CAS  PubMed  Google Scholar 

  • Mamiya A, Nadim F (2004) Dynamic interaction of oscillatory neurons coupled with reciprocally inhibitory synapses acts to stabilize the rhythm period. J Neurosci 24:5140–5150

    Article  CAS  PubMed  Google Scholar 

  • Marder E, Bucher D (2005) Robustness in neuronal systems: the balance between homeostasis, plasticity, and modulation. In: Jen E (ed) Robust design: a repertoire of biological, ecological and engineering case studies. Oxford University Press, Oxford

    Google Scholar 

  • Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291–316

    Article  CAS  PubMed  Google Scholar 

  • Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687–717

    CAS  PubMed  Google Scholar 

  • Marder E, Thirumalai V (2002) Cellular, synaptic and network effects of neuromodulation. Neural Netw 15:479–493

    Article  PubMed  Google Scholar 

  • Marder E, Weimann JM (1992) Modulatory control of multiple task processing in the stomatogastric nervous system. Pergamon Press, New York

    Google Scholar 

  • Marder E, Hooper SL, Siwicki KK (1986) Modulatory action and distribution of the neuropeptide proctolin in the crustacean stomatogastric nervous system. J Comp Neurol 243:454–467

    Article  CAS  PubMed  Google Scholar 

  • Marder E, Calabrese RL, Nusbaum MP, Trimmer B (1987) Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous systems of the rock crab, Cancer borealis, and the spiny lobster, Panulirus interruptus. J Comp Neurol 259:150–163

    Article  CAS  PubMed  Google Scholar 

  • Marder E, Jorge-Rivera JC, Kilman V, Weimann JM (1997) Peptidergic modulation of synaptic transmission in a rhythmic motor system. Advances in organ biology. JAI Press, Greenwich, CT, pp 213–233

    Google Scholar 

  • Marder E, Blitz DM, Christie AE, Nusbaum MP (2002) Convergence and divergence of cotransmitter systems in the crab stomatogastric nervous system. In: Wiese K (ed) The crustacean nervous system. Springer, Berlin

  • Marder E, Bucher D, Schulz DJ, Taylor AL (2005) Invertebrate central pattern generation moves along. Curr Biol 15:R685–R699

    Article  CAS  PubMed  Google Scholar 

  • Maynard DM, Dando MR (1974) The structure of the stomatogastric neuromuscular system in Callinectes sapidus, Homarus americanus and Panulirus argus (Decapoda Crustacea). Philos Trans R Soc Lond B Biol Sci 268:161–220

    Article  CAS  PubMed  Google Scholar 

  • Meyrand P, Marder E (1991) Matching neural and muscle oscillators: control by FMRFamide-like peptides. J Neurosci 11:1150–1161

    CAS  PubMed  Google Scholar 

  • Meyrand P, Simmers J, Moulins M (1991) Construction of a pattern-generating circuit with neurons of different networks. Nature 351:60–63

    Article  CAS  PubMed  Google Scholar 

  • Meyrand P, Weimann JM, Marder E (1992) Multiple axonal spike initiation zones in a motor neuron: serotonin activation. J Neurosci 12:2803–2812

    CAS  PubMed  Google Scholar 

  • Meyrand P, Simmers J, Moulins M (1994) Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system. J Neurosci 14:630–644

    CAS  PubMed  Google Scholar 

  • Montague PR, Hyman SE, Cohen JD (2004) Computational roles for dopamine in behavioural control. Nature 431:760–767

    Article  CAS  PubMed  Google Scholar 

  • Morris LG, Hooper SL (2001) Mechanisms underlying stabilization of temporally summated muscle contractions in the lobster (Panulirus) pyloric system. J Neurophysiol 85:254–268

    CAS  PubMed  Google Scholar 

  • Msghina M, Govind CK, Atwood HL (1998) Synaptic structure and transmitter release in crustacean phasic and tonic motor neurons. J Neurosci 18:1374–1382

    CAS  PubMed  Google Scholar 

  • Mulloney B, Hall WM (1991) Neurons with histamine-like immunoreactivity in the segmental and stomatogastric nervous systems of the crayfish Pacifastacus leniusculus and the lobster Homarus americanus. Cell Tissue Res 266:197–207

    Article  CAS  PubMed  Google Scholar 

  • Norris BJ, Coleman MJ, Nusbaum MP (1994) Recruitment of a projection neuron determines gastric mill motor pattern selection in the stomatogastric nervous system of the crab, Cancer borealis. J Neurophysiol 72:1451–1463

    CAS  PubMed  Google Scholar 

  • Norris BJ, Coleman MJ, Nusbaum MP (1996) Pyloric motor pattern modification by a newly identified projection neuron in the crab stomatogastric nervous system. J Neurophysiol 75:97–108

    CAS  PubMed  Google Scholar 

  • Nusbaum MP (1986) Synaptic basis of swim initiation in the leech. III. Synaptic effects of serotonin-containing interneurones (cells 21 and 61) on swim CPG neurones (cells 18 and 208). J Exp Biol 122:303–321

    CAS  PubMed  Google Scholar 

  • Nusbaum MP (2002) Regulating peptidergic modulation of rhythmically active neural circuits. Brain Behav Evol 60:378–387

    Article  PubMed  Google Scholar 

  • Nusbaum MP, Beenhakker MP (2002) A small-systems approach to motor pattern generation. Nature 417:343–350

    Article  CAS  PubMed  Google Scholar 

  • Nusbaum MP, Marder E (1989a) A modulatory proctolin-containing neuron (MPN). I. Identification and characterization. J Neurosci 9:1591–1599

    CAS  PubMed  Google Scholar 

  • Nusbaum MP, Marder E (1989b) A modulatory proctolin-containing neuron (MPN). II. State-dependent modulation of rhythmic motor activity. J Neurosci 9:1600–1607

    CAS  PubMed  Google Scholar 

  • Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E (2001) The roles of co-transmission in neural network modulation. Trends Neurosci 24:146–154

    Article  CAS  PubMed  Google Scholar 

  • Powers LW (1973) Gastric mill rhythms in intact crabs. Comp Biochem Physiol 46:767–783

    Article  Google Scholar 

  • Prinz AA, Billimoria CP, Marder E (2003a) Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. J Neurophysiol 90:3998–4015

    Article  PubMed  Google Scholar 

  • Prinz AA, Thirumalai V, Marder E (2003b) The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. J Neurosci 23:943–954

    CAS  PubMed  Google Scholar 

  • Prinz AA, Bucher D, Marder E (2004) Similar network activity from disparate circuit parameters. Nat Neurosci 7:1345–1352

    Article  CAS  PubMed  Google Scholar 

  • Pulver SR, Marder E (2002) Neuromodulatory complement of the pericardial organs in the embryonic lobster, Homarus americanus. J Comp Neurol 451:79–90

    Article  CAS  PubMed  Google Scholar 

  • Qian SM, Delaney KR (1997) Neuromodulation of activity-dependent synaptic enhancement at crayfish neuromuscular junction. Brain Res 771:259–270

    Article  CAS  PubMed  Google Scholar 

  • Ramirez JM, Viemari JC (2005) Determinants of inspiratory activity. Respir Physiol Neurobiol 147:145–157

    Article  CAS  PubMed  Google Scholar 

  • Reed RA, Page CH (1977) Circumesophageal connective control of the common inhibitory motoneuron in the crab, Carcinus maenas. Comp Biochem Physiol 56:567–571

    Article  Google Scholar 

  • Rehm KJ, Deeg KE, Marder E (2008) Developmental regulation of neuromodulator function in the stomatogastric ganglion of the lobster, Homarus americanus. J Neurosci 28:9828–9839

    Article  CAS  PubMed  Google Scholar 

  • Russell DF, Hartline DK (1981) A multiaction synapse evoking both EPSPs and enhancement of endogenous bursting. Brain Res 223:19–38

    Article  CAS  PubMed  Google Scholar 

  • Saghatelyan A, Roux P, Migliore M, Rochefort C, Desmaisons D, Charneau P, Shepherd GM, Lledo PM (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46:103–116

    Article  CAS  PubMed  Google Scholar 

  • Schulz DJ, Goaillard JM, Marder E (2006) Variable channel expression in identified single and electrically coupled neurons in different animals. Nat Neurosci 9:356–362

    Article  CAS  PubMed  Google Scholar 

  • Seal RP, Edwards RH (2006) Functional implications of neurotransmitter co-release: glutamate and GABA share the load. Curr Opin Pharmacol 6:114–119

    Article  CAS  PubMed  Google Scholar 

  • Selverston AI, Moulins M (1987) The crustacean stomatogastric system: a model for the study of central nervous systems. Springer-Verlag, Heidelberg

    Google Scholar 

  • Sen K, Jorge-Rivera JC, Marder E, Abbott LF (1996) Decoding synapses. J Neurosci 16:6307–6318

    CAS  PubMed  Google Scholar 

  • Sigvardt KA, Mulloney B (1982a) Properties of synapses made by IVN command-interneurones in the stomatogastric ganglion of the spiny lobster Panulirus interruptus. J Exp Biol 97:153–168

    CAS  PubMed  Google Scholar 

  • Sigvardt KA, Mulloney B (1982b) Sensory alteration of motor patterns in the stomatogastric nervous system of the spiny lobster Panulirus interruptus. J Exp Biol 97:137–152

    CAS  PubMed  Google Scholar 

  • Skiebe P (2001) Neuropeptides are ubiquitous chemical mediators: using the stomatogastric nervous system as a model system. J Exp Biol 204:2035–2048

    CAS  PubMed  Google Scholar 

  • Skiebe P (2003) Neuropeptides in the crayfish stomatogastric nervous system. Microsc Res Tech 60:302–312

    Article  CAS  PubMed  Google Scholar 

  • Skiebe P, Schneider H (1994) Allatostatin peptides in the crab stomatogastric nervous system: inhibition of the pyloric motor pattern and distribution of allatostatin-like immunoreactivity. J Exp Biol 194:195–208

    CAS  PubMed  Google Scholar 

  • Skiebe P, Wollenschlager T (2002) Putative neurohemal release zones in the stomatogastric nervous system of decapod crustaceans. J Comp Neurol 453:280–291

    Article  PubMed  Google Scholar 

  • Skiebe P, Dreger M, Meseke M, Evers JF, Hucho F (2002) Identification of orcokinins in single neurons in the stomatogastric nervous system of the crayfish, Cherax destructor. J Comp Neurol 444:245–259

    Article  CAS  PubMed  Google Scholar 

  • Smarandache CR, Stein W (2007) Sensory-induced modification of two motor patterns in the crab, Cancer pagurus. J Exp Biol 210:2912–2922

    Article  CAS  PubMed  Google Scholar 

  • Spirito CP (1975) The organization of the crayfish oesophageal nervous system. J Comp Physiol A 102:237–249

    Article  Google Scholar 

  • Spitzer N, Cymbalyuk G, Zhang H, Edwards DH, Baro DJ (2008a) Serotonin transduction cascades mediate variable changes in pyloric network cycle frequency in response to the same modulatory challenge. J Neurophysiol 99:2844–2863

    Article  CAS  PubMed  Google Scholar 

  • Spitzer N, Edwards DH, Baro DJ (2008b) Conservation of structure, signaling and pharmacology between two serotonin receptor subtypes from decapod crustaceans, Panulirus interruptus and Procambarus clarkii. J Exp Biol 211:92–105

    Article  CAS  PubMed  Google Scholar 

  • Stein W, Eberle CC, Hedrich UBS (2005) Motor pattern selection by nitric oxide in the stomatogastric nervous system of the crab. Eur J Neurosci 21:2767–2781

    Article  PubMed  Google Scholar 

  • Stein W, Smarandache CR, Nickmann M, Hedrich UB (2006) Functional consequences of activity-dependent synaptic enhancement at a crustacean neuromuscular junction. J Exp Biol 209:1285–1300

    Article  PubMed  Google Scholar 

  • Stein W, DeLong ND, Wood DE, Nusbaum MP (2007) Divergent co-transmitter actions underlie motor pattern activation by a modulatory projection neuron. Eur J Neurosci 26:1148–1165

    Article  PubMed  Google Scholar 

  • Stemmler EA, Peguero B, Bruns EA, Dickinson PS, Christie AE (2007) Identification, physiological actions, and distribution of TPSGFLGMRamide: a novel tachykinin-related peptide from the midgut and stomatogastric nervous system of Cancer crabs. J Neurochem 101:1351–1366

    Article  CAS  PubMed  Google Scholar 

  • Swensen AM, Marder E (2000) Multiple peptides converge to activate the same voltage-dependent current in a central pattern-generating circuit. J Neurosci 20:6752–6759

    CAS  PubMed  Google Scholar 

  • Swensen AM, Marder E (2001) Modulators with convergent cellular actions elicit distinct circuit outputs. J Neurosci 21:4050–4058

    CAS  PubMed  Google Scholar 

  • Swensen AM, Golowasch J, Christie AE, Coleman MJ, Nusbaum MP, Marder E (2000) GABA and responses to GABA in the stomatogastric ganglion of the crab Cancer borealis. J Exp Biol 203:2075–2092

    CAS  PubMed  Google Scholar 

  • Taylor AL, Goaillard JM, Marder E (2009) How multiple conductances determine electrophysiological properties in a multicompartment model. J Neurosci 29:5573–5586

    Article  CAS  PubMed  Google Scholar 

  • Thirumalai V, Prinz AA, Johnson CD, Marder E (2006) Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period. J Neurophysiol 95:1762–1770

    Article  CAS  PubMed  Google Scholar 

  • Thoby-Brisson M, Simmers J (1998) Neuromodulatory inputs maintain expression of a lobster motor pattern-generating network in a modulation-dependent state: evidence from long-term decentralization in vitro. J Neurosci 18:2212–2225

    CAS  PubMed  Google Scholar 

  • Thoby-Brisson M, Simmers J (2002) Long-term neuromodulatory regulation of a motor pattern-generating network: maintenance of synaptic efficacy and oscillatory properties. J Neurophysiol 88:2942–2953

    Article  PubMed  Google Scholar 

  • Tierney AJ, Blanck J, Mercier J (1997) FMRFamide-like peptides in the crayfish (Procambarus clarkii) stomatogastric nervous system: distribution and effects on the pyloric motor pattern. J Exp Biol 200:3221–3233

    CAS  PubMed  Google Scholar 

  • Tobin AE, Calabrese RL (2005) Myomodulin increases Ih and inhibits the NA/K pump to modulate bursting in leech heart interneurons. J Neurophysiol 94:3938–3950

    Article  CAS  PubMed  Google Scholar 

  • Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221–227

    Article  CAS  PubMed  Google Scholar 

  • Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97–107

    Article  CAS  PubMed  Google Scholar 

  • Turrigiano G, Abbott LF, Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974–977

    Article  CAS  PubMed  Google Scholar 

  • Turrigiano G, LeMasson G, Marder E (1995) Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons. J Neurosci 15:3640–3652

    CAS  PubMed  Google Scholar 

  • von Bohlen und Halbach O, Dermietzel R (2006) Neurotransmitters and neuromodulators: handbook of receptors and biological effects. Wiley, New York

  • Weimann JM, Marder E, Evans B, Calabrese RL (1993) The effects of SDRNFLRFamide and TNRNFLRFamide on the motor patterns of the stomatogastric ganglion of the crab Cancer borealis. J Exp Biol 181:1–26

    CAS  PubMed  Google Scholar 

  • Weimann JM, Skiebe P, Heinzel HG, Soto C, Kopell N, Jorge-Rivera JC, Marder E (1997) Modulation of oscillator interactions in the crab stomatogastric ganglion by crustacean cardioactive peptide. J Neurosci 17:1748–1760

    CAS  PubMed  Google Scholar 

  • Wood DE, Nusbaum MP (2002) Extracellular peptidase activity tunes motor pattern modulation. J Neurosci 22:4185–4195

    CAS  PubMed  Google Scholar 

  • Wood DE, Stein W, Nusbaum MP (2000) Projection neurons with shared cotransmitters elicit different motor patterns from the same neural circuit. J Neurosci 20:8943–8953

    CAS  PubMed  Google Scholar 

  • Wood DE, Manor Y, Nadim F, Nusbaum MP (2004) Intercircuit control via rhythmic regulation of projection neuron activity. J Neurosci 24:7455–7463

    Article  CAS  PubMed  Google Scholar 

  • Worden MK, Bykhovskaia M, Hackett JT (1997) Facilitation at the lobster neuromuscular junction: a stimulus-dependent mobilization model. J Neurophysiol 78:417–428

    CAS  PubMed  Google Scholar 

  • Zhang B, Harris-Warrick RM (1994) Multiple receptors mediate the modulatory effects of serotonergic neurons in a small neural network. J Exp Biol 190:55–77

    CAS  PubMed  Google Scholar 

  • Zhang B, Harris-Warrick RM (1995) Calcium-dependent plateau potentials in a crab stomatogastric ganglion motor neuron. I. Calcium current and its modulation by serotonin. J Neurophysiol 74:1929–1937

    CAS  PubMed  Google Scholar 

  • Zhang B, Wootton JF, Harris-Warrick RM (1995) Calcium-dependent plateau potentials in a crab stomatogastric ganglion motor neuron. II. Calcium-activated slow inward current. J Neurophysiol 74:1938–1946

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I thank M.P. Nusbaum, F. Nadim and H. Wolf for critically reading the manuscript and polishing the English. I would also like to thank N. Daur, U. Hedrich and J. Ausborn for helpful discussions. Research support in our laboratory is from German Research Foundation (DFG) grants.

Author information

Authors and Affiliations

  1. Institute of Neurobiology, Ulm University, 89069, Ulm, Germany

    Wolfgang Stein

Authors
  1. Wolfgang Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wolfgang Stein.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental 1 (DOC 229 kb)

Supplemental 2 (DOC 1809 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stein, W. Modulation of stomatogastric rhythms. J Comp Physiol A 195, 989–1009 (2009). https://doi.org/10.1007/s00359-009-0483-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-009-0483-y

Keywords

Search

Navigation