Skip to main content
SpringerLink
Log in

Differing synaptic strengths between homologous mechanosensory neurons

  • Original Paper
  • Published:
Invertebrate Neuroscience

Abstract

Leeches have four mechanosensory pressure neurons (P cells) in each midbody ganglion. Within a ganglion, P cells show complex electrical and chemical connections that vary between species. In Hirudo verbana, stimulating one P cell causes a weak depolarization followed by a strong hyperpolarization in the other P cells; however, stimulating a P cell in Erpobdella obscura produces strong depolarizations in the other P cells. In this study, we examined interactions between P cells in the American medicinal leech Macrobdella decora. Not only is Macrobdella more closely related to Hirudo than to Erpobdella, but Hirudo and Macrobdella also have very similar behavioral responses to mechanical stimulation. Despite the phylogenetic relationship and behavioral similarities between the two species, we found that intracellular stimulation of one P cell in Macrobdella causes a depolarization in the other P cells, rather than the hyperpolarization seen in Hirudo. Experiments performed in a high Mg2+, 0 Ca2+ saline solution and a high Mg2+, high Ca2+ saline solution suggest that the P cells in Macrobdella have a monosynaptic excitatory connection, a polysynaptic inhibitory connection, and a weak electrical coupling, similar to the connections between P cells in Hirudo. The difference in net response of P cells between these two species seems to be based on differences in the strengths of the chemical connections. These results demonstrate that even when behavioral patterns are conserved in closely related species, the underlying neural circuitry is not necessarily tightly constrained.

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

Similar content being viewed by others

References

  • Baca SM, Marin-Burgin A, Wagenaar DA, Kristan WB Jr (2008) Widespread inhibition proportional to excitation controls the gain of a leech behavioral circuit. Neuron 57:276–289

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Baltzley MJ, Gaudry Q, Kristan WB Jr (2010) Species-specific behavioral patterns correlate with differences in synaptic connections between homologous mechanosensory neurons. J Comp Physiol A 196:181–197

    Article  Google Scholar 

  • Baylor DA, Nicholls JG (1969) Chemical and electrical synaptic connexions between cutaneous mechanoreceptor neurones in the central nervous system of the leech. J Physiol 203:591–609

    PubMed  CAS  PubMed Central  Google Scholar 

  • Berman SL (1985) Convergent evolution in the hindlimb of bipedal rodents. J Zool Syst Evol Res 23:59–77

    Article  Google Scholar 

  • Borda E, Siddall ME (2004) Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Mol Phylogenet Evol 30:213–225

    Article  PubMed  CAS  Google Scholar 

  • Breidbach O, Kutsch W (1995) Introductory remarks. In: Breidbach O, Kutsch W (eds) The nervous system of invertebrates: an evolutionary and comparative approach. Birkhauser Verlag, Basel, pp 1–6

    Google Scholar 

  • Chiang JTA, Steciuk M, Shtonda B, Avery L (2006) Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes. J Exp Biol 209:1859–1873

    Article  PubMed  Google Scholar 

  • Dacks AM, Christensen TA, Hildebrand JG (2006) Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727–746

    Article  PubMed  CAS  Google Scholar 

  • Elsas SM, Kwak EM, Stent GS (1995) Acetylcholine-induced retraction of an identified axon in the developing leech embryo. J Neurosci 15:1419–1436

    PubMed  CAS  Google Scholar 

  • Envoy WH, Cohen MJ (1969) Sensory and motor interactions in the locomotor reflexes of crabs. J Exp Biol 51:151–169

    Google Scholar 

  • Fahey PK, Burkhardt DA (2003) Center-surround organization in bipolar cells: symmetry for opposing contrasts. Vis Neurosci 20:1–10

    Article  PubMed  Google Scholar 

  • Fenelon VS, LeFeuvre Y, Meyrand P (2004) Phylogenetic, ontogenetic and adult adaptive plasticity of rhythmic neural networks: a common neuromodulatory mechanism? J Comp Physiol A 190:691–705

    Article  CAS  Google Scholar 

  • Gaudry Q, Ruiz N, Huang T, Kristan WB III, Kristan WB Jr (2010) Behavioral choice across leech species: chacun à son goût. J Exp Biol 213:1356–1365

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Grider JR, Jin JG (1994) Distinct populations of sensory neurons mediate the peristaltic reflex elicited by muscle stretch and mucosal stimulation. J Neurosci 14:2854–2860

    PubMed  CAS  Google Scholar 

  • Hill ES, Blagburn JM (1998) Indirect synaptic inputs from filiform hair sensory neurons contribute to the receptive fields of giant interneurons in the first-instar cockroach. J Comp Physiol A 183:467–476

    Article  PubMed  CAS  Google Scholar 

  • Johansen J, Kleinhaus AL (1990) Ionic conductances in two types of sensory neurons in the leech, Macrobdella decora. Comp Biochem Physiol 97A:577–582

    Article  Google Scholar 

  • Katz PS (2011) Neural mechanisms underlying the evolvability of behaviour. Phil Trans R Soc B 366:2086–2099

    Article  PubMed  PubMed Central  Google Scholar 

  • Katz PS, Fickbohm DJT, Lynn-Bullock CP (2001) Evidence that the central pattern generator for swimming in Tritonia arose from a non-rhythmic neuromodulatory arousal system: Implications for the evolution of specialized behavior. Am Zool 41:962–975

    Article  Google Scholar 

  • Kawasaki M (1993) Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus. J Comp Physiol A 173:9–22

    Article  PubMed  CAS  Google Scholar 

  • Kramer AP, Goldman JR (1981) The nervous system of the glossiphoniid leech Haementeria ghilianii. 1 Identification of neurons. J Comp Physiol 144:435–448

    Article  Google Scholar 

  • Kramer AP, Stent GS (1985) Developmental arborization of sensory neurons in the leech Haementeria ghilianii. 2. Experimentally induced variations in the branching pattern. J Neurosci 5:768–775

    PubMed  CAS  Google Scholar 

  • Kramer AP, Goldman JR, Stent GS (1985) Developmental arborization of sensory neurons in the leech Haementeria ghilianii. 1. Origin of natural variations in the branching pattern. J Neurosci 5:759–767

    PubMed  CAS  Google Scholar 

  • Kristan WB Jr (1982) Sensory and motor neurones responsible for the local bending response in leeches. J Exp Biol 96:161–180

    Google Scholar 

  • Kristan WB Jr, McGirr SJ, Simpson GV (1982) Behavioral and mechanosensory neurone responses to skin stimulation in leeches. J Exp Biol 96:143–160

    Google Scholar 

  • Lent CM, Frazer BM (1977) Connectivity of monoamine-containing neurones in central nervous system of leech. Nature 266:844–847

    Article  PubMed  CAS  Google Scholar 

  • Lockery SR, Kristan WB Jr (1990a) Distributed processing of sensory information in the leech. I. Input-output relations of the local bending reflex. J Neurosci 10:1811–1815

    PubMed  CAS  Google Scholar 

  • Lockery SR, Kristan WB Jr (1990b) Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex. J Neurosci 10:1816–1829

    PubMed  CAS  Google Scholar 

  • Marin-Burgin A, Eisenhart FJ, Kristan WB Jr, French KA (2006) Embryonic electrical connections appear to pre-figure a behavioral circuit in the leech CNS. J Comp Physiol A 192:123–133

    Article  Google Scholar 

  • Newcomb JM, Katz PS (2007) Homologs of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors. J Comp Physiol A 193:425–443

    Article  CAS  Google Scholar 

  • Nicholls JG, Baylor DA (1968) Specific modalities and receptive fields of sensory neurons in CNS of the leech. J Neurophysiol 31:740–756

    PubMed  CAS  Google Scholar 

  • Nobili R, Mammano F, Ashmore J (1998) How well do we understand the cochlea? Trends Neurosci 21:159–167

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nusbaum MP, Kristan WB Jr (1986) Swim initiation in the leech by serotonin-containing interneurons, cells 21 and 61. J Exp Biol 122:277–302

    PubMed  CAS  Google Scholar 

  • Sakurai A, Newcomb JM, Lillvis JL, Katz PS (2011) Different roles for homologous interneurons in species exhibiting similar rhythmic behaviors. Curr Biol 21:1036–1043

    Article  PubMed  CAS  Google Scholar 

  • Siddall ME, Apakupakul K, Burreson EM, Coates KA, Erseus C, Gelder SR, Kallersjo M, Trapido-Rosenthal H (2001) Validating Livanow: molecular data agree that leeches, branchiobdellidans, and Acanthobdella peledina form a monophyletic group of oligochaetes. Mol Phylogenet Evol 21:346–351

    Article  PubMed  CAS  Google Scholar 

  • Siddall ME, Trontelj P, Utevsky SY, Nkamany M, Macdonald KS (2007) Diverse molecular data demonstrate that commercially available medicinal leeches are not Hirudo medicinalis. Proc Roy Soc B 274:1481–1487

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank K. L. Todd and S. D. Rees for assistance with data collection. We thank W. B. Kristan, Jr. for providing laboratory space and resources. We thank M. P. LeMaster for feedback on the manuscript. Support for K. R. Gibbons was provided by an REU to the National Science Foundation Grant IOB-0523959 to W. B. Kristan, Jr. and K. A. Mesce. Support for M. J. Baltzley was provided by a Faculty Development Grant from St. Mary’s College of Maryland.

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Department of Biology, St. Mary’s College of Maryland, St. Mary’s City, MD, 20686-3001, USA

    Kaitlin R. Gibbons & Michael J. Baltzley

  2. Department of Biology, Western Oregon University, Monmouth, OR, 97361, USA

    Michael J. Baltzley

Authors
  1. Kaitlin R. Gibbons
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael J. Baltzley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael J. Baltzley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gibbons, K.R., Baltzley, M.J. Differing synaptic strengths between homologous mechanosensory neurons. Invert Neurosci 14, 103–111 (2014). https://doi.org/10.1007/s10158-014-0168-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10158-014-0168-2

Keywords

Search

Navigation