Skip to main content

Artificial synaptic modification reveals a dynamical invariant in the pyloric CPG

European Journal of Applied Physiology volume 102, pages 667–675 (2008)Cite this article

Abstract

The sequential firing of neurons in central pattern generators (CPGs) is generally thought to be a result of an interaction between intrinsic cellular and synaptic properties of the component neurons. Due to experimental limitations, it is usually difficult to address the role of each of these properties separately. We have done so by using the crustacean stomatogastric CPG and the dynamic clamp technique to measure how the network responds to the selective modification of an individual important synapse. Our results show that the burst periods and the phase lags between the constrictor (LP) and dilator (PD) neurons across preparations showed significant variability during equivalent experimental manipulations. Despite this variability, the ratio between the change in the burst period and the change in the phase lag between the same neurons was tightly preserved in all preparations, revealing a dynamical invariant in the system. This dynamical invariant was preserved despite the individual variability in the period and phase lag measurements, suggesting a tightly regulated constraint between the parameters of the network.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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

References

  • Altringham JD, Ellerby DJ (1999) Fish swimming: patterns in muscle function. J Exp Biol 202:3397–3403

    PubMed  CAS  Google Scholar 

  • Braun G, Mulloney B (1993) Cholinergic modulation of the swimmeret motor system in crayfish. J Neurophysiol 70:2391–2398

    PubMed  CAS  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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Delcomyn F (1980) Neural basis of rhythmic behavior in animals. Science 210:492–498

    PubMed  Article  CAS  Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1:195–230

    PubMed  Article  CAS  Google Scholar 

  • Dicaprio R, Jordan G, Hampton T (1997) Maintenance of motor pattern phase relationships in the ventilatory system of the crab. J Exp Biol 200:963–974

    PubMed  Google Scholar 

  • Eisen JS, Marder E (1984) A mechanism for production of phase shifts in a pattern generator. J Neurophysiol 51:1375–1393

    PubMed  CAS  Google Scholar 

  • Elson RC, Huerta R, Abarbanel HD, Rabinovich MI, Selverston AI (1999) Dynamic control of irregular bursting in an identified neuron of an oscillatory circuit. J Neurophysiol 82:115–122

    PubMed  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    Google Scholar 

  • Hooper SL (1997a) Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion. J Comput Neurosci 4:191–205

    PubMed  Article  CAS  Google Scholar 

  • Hooper SL (1997b) The pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion comprises two phase-maintaining subsets. J Comput Neurosci 4:207–219

    PubMed  Article  CAS  Google Scholar 

  • Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837–3847

    PubMed  CAS  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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7:563–574

    PubMed  Article  CAS  Google Scholar 

  • Marder E, Prinz AA (2002) Modeling stability in neuron and network function: the role of activity in homeostasis. Bioessays 24:1145–1154

    PubMed  Article  CAS  Google Scholar 

  • Nadim F, Manor Y (2000) The role of short-term synaptic dynamics in motor control. Curr Opin Neurobiol 10:683–690

    PubMed  Article  CAS  Google Scholar 

  • Nowotny T, Szucs A, Pinto RD, Selverston AI (2006) StdpC: a modern dynamic clamp. J Neurosci Methods 158(2):287–299

    PubMed  Article  Google Scholar 

  • Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O (2006) Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26:7523–7531

    PubMed  Article  CAS  Google Scholar 

  • Perez-Otano I, Ehlers MD (2005) Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci 28:229–238

    PubMed  Article  CAS  Google Scholar 

  • Pinto RD, Elson RC, Szucs A, Rabinovich MI, Selverston AI, Abarbanel HDI (2001) Extended dynamic clamp: controlling up to four neurons using a single desktop computer and interface. J Neurosci Methods 108:39–48

    PubMed  Article  CAS  Google Scholar 

  • Prinz AA, Abbott LF, Marder E (2004a) The dynamic clamp comes of age. Trends Neurosci 27:218–224

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Rabbah P, Nadim F (2005) Synaptic dynamics do not determine proper phase of activity in a central pattern generator. J Neurosci 25:11269–11278

    PubMed  Article  CAS  Google Scholar 

  • Raper JA (1979) Nonimpulsive-mediated synaptic transmission during the generation of a cyclic motor program. Science 205(4403):304–306

    PubMed  Article  CAS  Google Scholar 

  • Robinson HP, Kawai N (1993) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49:157–165

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Selverston AI, Moulins M (1987) The crustacean stomatogastric system. Springer, Berlin

    Google Scholar 

  • Sharp AA, O’Neil MB, Abbott LF, Marder E (1993a) The dynamic clamp: artificial conductances in biological neurons. Trends Neurosci 16:389–394

    PubMed  Article  CAS  Google Scholar 

  • Sharp AA, O’Neil MB, Abbott LF, Marder E (1993b) Dynamic clamp: computer-generated conductances in real neurons. J Neurophysiol 69:992–995

    PubMed  CAS  Google Scholar 

  • Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349–374

    PubMed  Article  CAS  Google Scholar 

  • Stemmler M, Koch C (1999) How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate. Nat Neurosci 2:521–527

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Weaver AL, Hooper SL (2003) Follower neurons in lobster (Panulirus interruptus) pyloric network regulate pacemaker period in complementary ways. J Neurophysiol 89:1327–1338

    PubMed  Article  Google Scholar 

Download references

Acknowledgement

This research was supported by NIH grant R01 NS050945.

Author information

Affiliations

  1. Institute for Nonlinear Science (INLS), University of California, San Diego, 9500 Gilman Drive, Rm. 1G CMRR Bldg, La Jolla, CA, 92093-0402, USA

    Marcelo B. Reyes, Ramón Huerta, Mikhail I. Rabinovich & Allen I. Selverston

Authors
  1. Marcelo B. Reyes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramón Huerta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mikhail I. Rabinovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Allen I. Selverston
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcelo B. Reyes.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Reyes, M.B., Huerta, R., Rabinovich, M.I. et al. Artificial synaptic modification reveals a dynamical invariant in the pyloric CPG. Eur J Appl Physiol 102, 667–675 (2008). https://doi.org/10.1007/s00421-007-0635-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-007-0635-0

Keywords

  • Central pattern generators
  • Dynamic clamp
  • Artificial synapse
  • Oscillatory rhythm
  • Variability of physiological parameters
  • Homeostasis