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:

Behavioral choice by presynaptic inhibition of tactile sensory terminals

Abstract

When presented with multiple stimuli, animals generally choose to respond only to one input. The neuronal mechanisms determining such behavioral choices are poorly understood. We found that the medicinal leech had greatly diminished responses to moderate mechanosensory input as it fed. Feeding dominated other responses by suppressing transmitter release from mechanosensory neurons onto all of their neuronal targets. The effects of feeding on synaptic transmission could be mimicked by serotonin. Furthermore, the serotonin antagonist mianserin blocked feeding-induced decreases in synaptic transmission. These results indicate that feeding predominates behaviors by using serotonin at an early stage of sensory processing, namely on presynaptic terminals of mechanosensory neurons.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Leech behavior and the semi-intact preparation.
Figure 2: Local bend motor responses during feeding and nonfeeding.
Figure 3: Feeding decreases the amplitudes of EPSPs at P cell synapses.
Figure 4: Increased PPR during feeding suggests a decrease in the probability of transmitter release at P-cell terminals.
Figure 5: Stimulation of swim-gating neurons elicits bouts of swimming during feeding.
Figure 6: Serotonin decreases the P cell–to–AP neuron synaptic potential amplitudes.
Figure 7: Serotonin mimics feeding by decreasing local bending.
Figure 8: Mianserin blocks feeding-induced depression of P-cell EPSPs and reduces local bending.

Similar content being viewed by others

References

  1. Poulet, J.F.A. & Hedwig, B. A corollary discharge maintains auditory sensitivity during sound production. Nature 418, 872–876 (2002).

    Article  CAS  Google Scholar 

  2. Murakami, M., Kashiwadani, H., Kirino, Y. & Mori, K. State-dependent sensory gating in olfactory cortex. Neuron 46, 285–296 (2005).

    Article  CAS  Google Scholar 

  3. Fields, H. State-dependent opioid control of pain. Nat. Rev. Neurosci. 5, 565–575 (2004).

    Article  CAS  Google Scholar 

  4. Sherrington, C. The Integrative Action of the Nervous System (Yale University Press, New Haven, Connecticut, 1906).

  5. Davis, W.J., Mpitsos, G.J. & Pinneo, J.M. The behavioral hierarchy of the mollusk Pleurobranchaea. I. The dominant position of the feeding behavior. J. Comp. Physiol. [A] 90, 207–224 (1974).

    Article  Google Scholar 

  6. Kristan, W.B. Jr. & Gillette, R. Behavioral Choice (eds. North, G. & Greenspan, R.) (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2007).

  7. Jing, J. & Gillette, R. Escape swim network interneurons have diverse roles in behavioral switching and putative arousal in Pleurobranchaea. J. Neurophysiol. 83, 1346–1355 (2000).

    Article  CAS  Google Scholar 

  8. Shaw, B.K. & Kristan, W.B. Jr. The neuronal basis of the behavioral choice between swimming and shortening in the leech: control is not selectively exercised at higher circuit levels. J. Neurosci. 17, 786–795 (1997).

    Article  CAS  Google Scholar 

  9. Baca, S.M., Marin-Burgin, A., Wagenaar, D.A. & Kristan, W.B. Jr. Widespread inhibition proportional to excitation controls the gain of a leech behavioral circuit. Neuron 57, 276–289 (2008).

    Article  CAS  Google Scholar 

  10. Olsen, S.R. & Wilson, R.I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956–960 (2008).

    Article  CAS  Google Scholar 

  11. Misell, L.M., Shaw, B.K. & Kristan, W.B. Jr. Behavioral hierarchy in the medicinal leech, Hirudo medicinalis: feeding as a dominant behavior. Behav. Brain Res. 90, 13–21 (1998).

    Article  CAS  Google Scholar 

  12. Wilson, R.J., Kristan, W.B. Jr. & Kleinhaus, A.L. An increase in activity of serotonergic Retzius neurones may not be necessary for the consummatory phase of feeding in the leech Hirudo medicinalis. J. Exp. Biol. 199, 1405–1414 (1996).

    CAS  PubMed  Google Scholar 

  13. Lockery, S.R. & Kristan, W.B. Jr. Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex. J. Neurosci. 10, 1816–1829 (1990).

    Article  CAS  Google Scholar 

  14. Shaw, B.K. & Kristan, W.B. Jr. Relative roles of the S cell network and parallel interneuronal pathways in the whole-body shortening reflex of the medicinal leech. J. Neurophysiol. 82, 1114–1123 (1999).

    Article  CAS  Google Scholar 

  15. Brodfuehrer, P.D. & Friesen, W.O. Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion. I. Output connections of Tr1 and Tr2. J. Comp. Physiol. [A] 159, 489–502 (1986).

    Article  CAS  Google Scholar 

  16. Groome, J.R., Vaughan, D.K. & Lent, C.M. Ingestive sensory inputs excite serotonin effector neurones and promote serotonin depletion from the leech central nervous system and periphery. J. Exp. Biol. 198, 1233–1242 (1995).

    CAS  PubMed  Google Scholar 

  17. Schulz, P.E., Cook, E.P. & Johnston, D. Using paired-pulse facilitation to probe the mechanisms for long-term potentiation (LTP). J. Physiol. (Paris) 89, 3–9 (1995).

    Article  CAS  Google Scholar 

  18. Kristan, W.B., Jr. Calabrese, R.L. & Friesen, W.O. Neuronal control of leech behavior. Prog. Neurobiol. 76, 279–327 (2005).

    Article  Google Scholar 

  19. Brodfuehrer, P.D., Debski, E.A., O'Gara, B.A. & Friesen, W.O. Neuronal control of leech swimming. J. Neurobiol. 27, 403–418 (1995).

    Article  CAS  Google Scholar 

  20. Weeks, J.C. & Kristan, W.B. Jr. Initiation, maintenance and modulation of swimming in the medicinal leech by the activity of a single neurone. J. Exp. Biol. 77, 71–88 (1978).

    Google Scholar 

  21. Puhl, J.G. & Mesce, K.A. Dopamine activates the motor pattern for crawling in the medicinal leech. J. Neurosci. 28, 4192–4200 (2008).

    Article  CAS  Google Scholar 

  22. Lockery, S.R. & Kristan, W.B. Jr. Two forms of sensitization of the local bending reflex of the medicinal leech. J. Comp. Physiol. [A] 168, 165–177 (1991).

    Article  CAS  Google Scholar 

  23. Lent, C.M. Serotonergic modulation of the feeding behavior of the medicinal leech. Brain Res. Bull. 14, 643–655 (1985).

    Article  CAS  Google Scholar 

  24. Norekian, T.P. & Satterlie, R.A. Serotonergic neural system not only activates swimming but also inhibits competing neural centers in a pteropod mollusc. Am. Zool. 41, 993–1000 (2001).

    Google Scholar 

  25. Ranganathan, R., Cannon, S.C. & Horvitz, H.R. MOD-1 is a serotonin-gated chloride channel that modulates locomotory behavior in C. elegans. Nature 408, 470–475 (2000).

    Article  CAS  Google Scholar 

  26. McNaughton, B.L. Long-term synaptic enhancement and short-term potentiation in rat fascia dentata act through different mechanisms. J. Physiol. (Lond.) 324, 249–262 (1982).

    Article  CAS  Google Scholar 

  27. Clarac, F. & Cattaert, D. Invertebrate presynaptic inhibition and motor control. Exp. Brain Res. 112, 163–180 (1996).

    Article  CAS  Google Scholar 

  28. Rudomin, P. & Schmidt, R.F. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp. Brain Res. 129, 1–37 (1999).

    Article  CAS  Google Scholar 

  29. Gold, J.I. & Shadlen, M.N. The neural basis of decision making. Annu. Rev. Neurosci. 30, 535–574 (2007).

    Article  CAS  Google Scholar 

  30. Machens, C.K., Romo, R. & Brody, C.D. Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science 307, 1121–1124 (2005).

    Article  CAS  Google Scholar 

  31. Wang, X.J. Decision making in recurrent neuronal circuits. Neuron 60, 215–234 (2008).

    Article  CAS  Google Scholar 

  32. Kupfermann, I. & Weiss, K.R. Motor program selection in simple model systems. Curr. Opin. Neurobiol. 11, 673–677 (2001).

    Article  CAS  Google Scholar 

  33. Fields, H.L. Understanding how opioids contribute to reward and analgesia. Reg. Anesth. Pain Med. 32, 242–246 (2007).

    Article  CAS  Google Scholar 

  34. Miyase, C.I., Kishi, R., de Freitas, R.L., Paz, D.A. & Coimbra, N.C. Involvement of pre- and postsynaptic serotonergic receptors of dorsal raphe nucleus neural network in the control of the sweet substance–induced analgesia in adult Rattus norvegicus (Rodentia, Muridae). Neurosci. Lett. 379, 169–173 (2005).

    Article  CAS  Google Scholar 

  35. Bucher, H.U. et al. Sucrose reduces pain reaction to heel lancing in preterm infants: a placebo-controlled, randomized and masked study. Pediatr. Res. 38, 332–335 (1995).

    Article  CAS  Google Scholar 

  36. Kavaliers, M. & Colwell, D.D. Sex differences in opioid and non-opioid mediated predator-induced analgesia in mice. Brain Res. 568, 173–177 (1991).

    Article  CAS  Google Scholar 

  37. Jankowska, E. Spinal interneuronal networks in the cat: elementary components. Brain Res. Rev. 57, 46–55 (2008).

    Article  Google Scholar 

  38. Shiba, K., Nakazawa, K., Ono, K. & Umezaki, T. Multifunctional laryngeal premotor neurons: their activities during breathing, coughing, sneezing and swallowing. J. Neurosci. 27, 5156–5162 (2007).

    Article  CAS  Google Scholar 

  39. Wilson, R.J. & Kleinhaus, A.L. Segmental control of midbody peristalsis during the consummatory phase of feeding in the medicinal leech, Hirudo medicinalis. Behav. Neurosci. 114, 635–646 (2000).

    Article  CAS  Google Scholar 

  40. Briggman, K.L. & Kristan, W.B. Jr. Imaging dedicated and multifunctional neural circuits generating distinct behaviors. J. Neurosci. 26, 10925–10933 (2006).

    Article  CAS  Google Scholar 

  41. Esch, T., Mesce, K.A. & Kristan, W.B. Evidence for sequential decision making in the medicinal leech. J. Neurosci. 22, 11045–11054 (2002).

    Article  CAS  Google Scholar 

  42. Lent, C.M. & Dickinson, M.H. Serotonin integrates the feeding behavior of the medicinal leech. J. Comp. Physiol. [A] 154, 457–471 (1984).

    Article  CAS  Google Scholar 

  43. Lent, C.M., Zundel, D., Freedman, E. & Groome, J.R. Serotonin in the leech central nervous system: anatomical correlates and behavioral effects. J. Comp. Physiol. [A] 168, 191–200 (1991).

    Article  CAS  Google Scholar 

  44. Zhang, X., Wilson, R.J., Li, Y. & Kleinhaus, A.L. Chemical and thermal stimuli have short-lived effects on the Retzius cell in the medicinal leech. J. Neurobiol. 43, 304–311 (2000).

    Article  CAS  Google Scholar 

  45. Ali, D.W., Catarsi, S. & Drapeau, P. Ionotropic and metabotropic activation of a neuronal chloride channel by serotonin and dopamine in the leech Hirudo medicinalis. J. Physiol. (Lond.) 509, 211–219 (1998).

    Article  CAS  Google Scholar 

  46. Catarsi, S. & Drapeau, P. Requirement for tyrosine phosphatase during serotonergic neuromodulation by protein kinase C. J. Neurosci. 17, 5792–5797 (1997).

    Article  CAS  Google Scholar 

  47. Kitson, S.L. 5-hydroxytryptamine (5-HT) receptor ligands. Curr. Pharm. Des. 13, 2621–2637 (2007).

    Article  CAS  Google Scholar 

  48. Dickinson, M.H. & Lent, C.M. Feeding behavior of the medicinal leech, Hirudo medicinalis L. J. Comp. Physiol. [A] 154, 449–455 (1984).

    Article  Google Scholar 

  49. Ort, C.A., Kristan, W.B. & Stent, G.S. Neuronal control of swimming in the medicinal leech. J. Comp. Physiol. [A] 94, 121–154 (1974).

    Article  Google Scholar 

Download references

Acknowledgements

The authors are extremely grateful to M. Scanziani for experimental suggestions and critical review of the manuscript. We would also like to thank K. Mesce for valuable editorial assistance and K. Todd for help with confocal microscopy and tissue processing. This work was supported by the US National Institutes of Health (MH43396 and NS35336 to W.B.K.) and the National Science Foundation (IOB-0523959 to K. Mesce and W.B.K.).

Author information

Authors and Affiliations

Authors

Contributions

Q.G. and W.B.K. designed the experiments and wrote the manuscript. Q.G. performed the experiments.

Corresponding author

Correspondence to William B Kristan Jr.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5 (PDF 6429 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gaudry, Q., Kristan, W. Behavioral choice by presynaptic inhibition of tactile sensory terminals. Nat Neurosci 12, 1450–1457 (2009). https://doi.org/10.1038/nn.2400

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2400

This article is cited by

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