Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Functional consequences of animal-to-animal variation in circuit parameters

Nature Neuroscience volume 12, pages 1424–1430 (2009)Cite this article

Abstract

How different are the neuronal circuits for a given behavior across individual animals? To address this question, we measured multiple cellular and synaptic parameters in individual preparations to see how they correlated with circuit function, using neurons and synapses in the pyloric circuit of the stomatogastric ganglion of the crab Cancer borealis. There was considerable preparation-to-preparation variability in the strength of two identified synapses, in the amplitude of a modulator-evoked current and in the expression of six ion channel genes. Nonetheless, we found strong correlations across preparations among these parameters and attributes of circuit performance. These data illustrate the importance of making multidimensional measurements from single preparations for understanding how variability in circuit output is related to the variability of multiple circuit parameters.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Variability of pyloric circuit output across crabs.
Figure 2: Variability of synaptic inputs to the LP neuron.
Figure 3: Variability of IMI in the LP neuron.
Figure 4: Correlations among synaptic current properties, IMI and LP neuron firing properties.
Figure 5: Correlations between mRNA expression and network output.

Similar content being viewed by others

References

  1. Prinz, A.A., Bucher, D. & Marder, E. Similar network activity from disparate circuit parameters. Nat. Neurosci. 7, 1345–1352 (2004).

    Article  CAS  Google Scholar 

  2. Goldman, M.S., Golowasch, J., Marder, E. & Abbott, L.F. Global structure, robustness and modulation of neuronal models. J. Neurosci. 21, 5229–5238 (2001).

    Article  CAS  Google Scholar 

  3. Achard, P. & De Schutter, E. Complex parameter landscape for a complex neuron model. PLoS Comput. Biol. 2, e94 (2006).

    Article  Google Scholar 

  4. Marder, E. & Goaillard, J.M. Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7, 563–574 (2006).

    Article  CAS  Google Scholar 

  5. Swensen, A.M. & Bean, B.P. Robustness of burst firing in dissociated purkinje neurons with acute or long-term reductions in sodium conductance. J. Neurosci. 25, 3509–3520 (2005).

    Article  CAS  Google Scholar 

  6. Golowasch, J., Abbott, L.F. & Marder, E. Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J. Neurosci. 19, RC33 (1999).

    Article  CAS  Google Scholar 

  7. Schulz, D.J., Goaillard, J.M. & Marder, E. Variable channel expression in identified single and electrically coupled neurons in different animals. Nat. Neurosci. 9, 356–362 (2006).

    Article  CAS  Google Scholar 

  8. Liss, B. et al. Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription. EMBO J. 20, 5715–5724 (2001).

    Article  CAS  Google Scholar 

  9. Liss, B. & Roeper, J. Correlating function and gene expression of individual basal ganglia neurons. Trends Neurosci. 27, 475–481 (2004).

    Article  CAS  Google Scholar 

  10. MacLean, J.N. et al. Activity-independent coregulation of IA and Ih in rhythmically active neurons. J. Neurophysiol. 94, 3601–3617 (2005).

    Article  Google Scholar 

  11. Schulz, D.J., Goaillard, J.M. & Marder, E.E. Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proc. Natl. Acad. Sci. USA 104, 13187–13191 (2007).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Harris-Warrick, R.M., Coniglio, L.M., Barazangi, N., Guckenheimer, J. & Gueron, S. Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J. Neurosci. 15, 342–358 (1995).

    Article  CAS  Google Scholar 

  15. Harris-Warrick, R.M., Coniglio, L.M., Levini, R.M., Gueron, S. & Guckenheimer, J. Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. J. Neurophysiol. 74, 1404–1420 (1995).

    Article  CAS  Google Scholar 

  16. Thuma, J.B., Harness, P.I., Koehnle, T.J., Morris, L.G. & Hooper, S.L. Muscle anatomy is a primary determinant of muscle relaxation dynamics in the lobster (Panulirus interruptus) stomatogastric system. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 193, 1101–1113 (2007).

    Article  Google Scholar 

  17. Golowasch, J. & Marder, E. Ionic currents of the lateral pyloric neuron of the stomatogastric ganglion of the crab. J. Neurophysiol. 67, 318–331 (1992).

    Article  CAS  Google Scholar 

  18. Taylor, A.L., Goaillard, J.M. & Marder, E. How multiple conductances determine electrophysiological properties in a multicompartmental model. J. Neurosci. 29, 5573–5586 (2009).

    Article  CAS  Google Scholar 

  19. Eisen, J.S. & Marder, E. 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 (1982).

    Article  CAS  Google Scholar 

  20. Marder, E. & Eisen, J.S. Transmitter identification of pyloric neurons: electrically coupled neurons use different neurotransmitters. J. Neurophysiol. 51, 1345–1361 (1984).

    Article  CAS  Google Scholar 

  21. Hooper, S.L. & Marder, E. Modulation of the lobster pyloric rhythm by the peptide proctolin. J. Neurosci. 7, 2097–2112 (1987).

    Article  CAS  Google Scholar 

  22. Miller, J.P. Pyloric mechanisms. in The Crustacean Stomatogastric System (eds. Selverston, A.I. & Moulins, M.) 109–145 (Springer-Verlag, Berlin, 1987).

  23. Thirumalai, V., Prinz, A.A., Johnson, C.D. & Marder, E. 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 (2006).

    Article  CAS  Google Scholar 

  24. Nadim, F., Manor, Y., Kopell, N. & Marder, E. Synaptic depression creates a switch that controls the frequency of an oscillatory circuit. Proc. Natl. Acad. Sci. USA 96, 8206–8211 (1999).

    Article  CAS  Google Scholar 

  25. Nusbaum, M.P., Blitz, D.M., Swensen, A.M., Wood, D. & Marder, E. The roles of co-transmission in neural network modulation. Trends Neurosci. 24, 146–154 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Swensen, A.M. & Marder, E. Modulators with convergent cellular actions elicit distinct circuit outputs. J. Neurosci. 21, 4050–4058 (2001).

    Article  CAS  Google Scholar 

  28. Golowasch, J. & Marder, E. Proctolin activates an inward current whose voltage dependence is modified by extracellular Ca2+. J. Neurosci. 12, 810–817 (1992).

    Article  CAS  Google Scholar 

  29. Weimann, J.M. et al. Modulation of oscillator interactions in the crab stomatogastric ganglion by crustacean cardioactive peptide. J. Neurosci. 17, 1748–1760 (1997).

    Article  CAS  Google Scholar 

  30. MacLean, J.N., Zhang, Y., Johnson, B.R. & Harris-Warrick, R.M. Activity-independent homeostasis in rhythmically active neurons. Neuron 37, 109–120 (2003).

    Article  CAS  Google Scholar 

  31. Lüthi, A. & McCormick, D.A. H-current: properties of a neuronal and network pacemaker. Neuron 21, 9–12 (1998).

    Article  Google Scholar 

  32. Norris, B.J., Weaver, A.L., Wenning, A., Garcia, P.S. & Calabrese, R.L. A central pattern generator producing alternative outputs: pattern, strength and dynamics of premotor synaptic input to leech heart motor neurons. J. Neurophysiol. 98, 2992–3005 (2007).

    Article  Google Scholar 

  33. Norris, B.J., Weaver, A.L., Wenning, A., Garcia, P.S. & Calabrese, R.L. A central pattern generator producing alternative outputs: phase relations of leech heart motor neurons with respect to premotor synaptic input. J. Neurophysiol. 98, 2983–2991 (2007).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  36. van Welie, I., van Hooft, J.A. & Wadman, W.J. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated Ih channels. Proc. Natl. Acad. Sci. USA 101, 5123–5128 (2004).

    Article  CAS  Google Scholar 

  37. Lien, C.C. & Jonas, P. Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J. Neurosci. 23, 2058–2068 (2003).

    Article  CAS  Google Scholar 

  38. Tierney, A.J. & Harris-Warrick, R.M. Physiological role of the transient potassium current in the pyloric circuit of the lobster stomatogastric ganglion. J. Neurophysiol. 67, 599–609 (1992).

    Article  CAS  Google Scholar 

  39. Rabbah, P. & Nadim, F. Distinct synaptic dynamics of heterogeneous pacemaker neurons in an oscillatory network. J. Neurophysiol. 97, 2239–2253 (2007).

    Article  Google Scholar 

  40. Greenspan, R.J. The flexible genome. Nat. Rev. Genet. 2, 383–387 (2001).

    Article  CAS  Google Scholar 

  41. Chouard, T. Darwin 200: beneath the surface. Nature 456, 300–303 (2008).

    Article  CAS  Google Scholar 

  42. Hooper, S.L. et al. 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 (1986).

    Article  CAS  Google Scholar 

  43. Weimann, J.M., Meyrand, P. & Marder, E. Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J. Neurophysiol. 65, 111–122 (1991).

    Article  CAS  Google Scholar 

  44. Buchholtz, F., Golowasch, J., Epstein, I.R. & Marder, E. Mathematical model of an identified stomatogastric ganglion neuron. J. Neurophysiol. 67, 332–340 (1992).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank S.R. Pulver and L.S. Tang for contributing data. This work was supported by US National Institutes of Health grants NS17813 (E.M.), MH46742 (E.M.) and NS50928 (A.L.T.), James S. McDonnell Foundation grant 220020065 (E.M.) and National Science Foundation grant IOB-0615160 (D.J.S.).

Author information

Author notes

  1. Jean-Marc Goaillard

    Present address: Present address: INSERM UMR 641, Faculté de Médecine-Secteur Nord, Université de la Méditerranée, Marseille, France.,

Authors and Affiliations

  1. Volen Center and Biology Department, Brandeis University, Waltham, Massachusetts, USA

    Jean-Marc Goaillard, Adam L Taylor & Eve Marder

  2. Biological Sciences, University of Missouri at Columbia, Columbia, Missouri, USA

    David J Schulz

Authors
  1. Jean-Marc Goaillard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam L Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David J Schulz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eve Marder
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.-M.G. conducted the majority of the electrophysiological experiments, analyzed data and contributed to writing the manuscript. A.L.T. analyzed data, conducted experiments and contributed to writing the manuscript. D.J.S. performed all of the quantitative single-cell PCR. E.M. supervised the experiments and contributed to writing the manuscript.

Corresponding author

Correspondence to Jean-Marc Goaillard.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3 (PDF 859 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goaillard, JM., Taylor, A., Schulz, D. et al. Functional consequences of animal-to-animal variation in circuit parameters. Nat Neurosci 12, 1424–1430 (2009). https://doi.org/10.1038/nn.2404

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2404

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing