Skip to main content
Log in

Pedal serotonergic neuron clusters of the pteropod mollusc, Clione limacina, contain two morphological subtypes with different innervation targets

  • Original Article
  • Published:
Invertebrate Neuroscience

Abstract

Each pedal ganglion of the pteropod mollusc Clione limacina contains a cluster of serotonin-immunoreactive neurons that have been shown to modulate contractions of the slow-twitch musculature of the wing-like parapodia, and contribute to swim accelerations. Each cluster has a variable number of neurons, between 5 and 9, but there is no significant difference between right and left ganglia. In experiments with electrophysiological recordings followed by dye-injection (carboxyfluorescein), the clusters were found to contain two subsets of neurons. The majority innervate the ipsilateral wing via nerve n4. Two of the neurons in each cluster send processes out of the pedal ganglion in nerves n3 and n8. The processes in nerve n3 innervate the body wall of the neck region, while those in nerve n8 innervate the body wall of the tail. The baseline electrophysiological activity of the two subsets of neurons was different as “wing” neurons had constant barrages of small synaptic activity, while the “body wall” neurons had few synaptic inputs. The potential roles of the Pd-SW cluster in swim acceleration (wing neurons) and control of fluid pressure in the body and wing hemocoelic compartments (body wall neurons) are discussed.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Ampatzis K, Song J, Ausborn J, El Manira A (2014) Separate microcircuit modules of distinct V2a interneurons and motoneurons control the speed of locomotion. Neuron 83:934–943

    CAS  PubMed  Google Scholar 

  • Arreola J, Calvo J, Garcia MC, Sanchez JA (1987) Modulation of calcium channels of twitch skeletal muscle fibers of the frog by adrenaline and cyclic adenosine monophosphate. J Physiol 393:307–330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985a) Control of locomotion in marine molluskClione limacina. I. Efferent activity during actual and fictitious swimming. Expl Brain Res 58:255–262

    Google Scholar 

  • Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985b) Control of locomotion in marine molluskClione limacina. II. Rhythmic neurons of pedal ganglia. Expl Brain Res 58:263–272

    Google Scholar 

  • Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985c) Control of locomotion in marine molluskClione limacina. III. On the origin of locomotory rhythm. Expl Brain Res 58:273–284

    Google Scholar 

  • Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985d) Control of locomotion in marine molluskClione limacina. IV. Role of type 12 interneurons. Expl Brain Res 58:285–293

    Google Scholar 

  • Arshavsky YI, Orlovsky GN, Panchin YV, Pavlova GA (1989) Control of locomotion in marine molluskClione limacina. VII. Reexamination of type 12 interneurons. Expl Brain Res 78:398–406

    Google Scholar 

  • Ausborn J, Mahmood R, El Manira A (2012) Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network. Proc Natl Acad Sci USA 109:E3631–E3639

    CAS  PubMed  Google Scholar 

  • Bjornfors ER, Picton LD, Song J, El Manira A (2019) Diversity of neurons and circuits controlling the speed of coordination of locomotion. Curr Opin Physiol 8:170–176

    Google Scholar 

  • Cairns SP, Borrani F (2015) β-Adrenergic modulation of skeletal muscle contraction: key role of excitation-contraction coupling. J Physiol 593:4713–4727

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dougherty KJ, Kiehn O (2010) Firing and cellular properties of V2a interneurons in the rodent spinal cord. J Neurosci 30:24–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dzoljic E, DeVries R, Dzoljic MR (1997) New and potent inhibitors of nitric oxide synthase reduce motor activity in mice. Behav Brain Res 87:209–212

    CAS  PubMed  Google Scholar 

  • Eklof-Ljunggren E, Haupt S, Ausborn J, Dehnisch I, Uhlen P, Higashijima S, El Manira A (2012) Origin of excitation underlying locomotion in the spinal circuit of zebrafish. Proc Natl Acad Sci USA 109:5511–5516

    PubMed  Google Scholar 

  • Emrick MA, Sadilek M, Konoki K, Catterall WA (2010) Beta-adrenergic-regulated phosphorylation of skeletal muscle Ca(V)1.1 channel in the fight-or-flight response. Proc Natl Acad Sci USA 43:18712–18717

    Google Scholar 

  • Gabriel JP, Mahmood R, Kyriakatos A, Soll I, Hauptmann G, Calabrese RL, El Manira A (2009) Serotonergic modulation of locomotion in zebrafish: endogenous release and synaptic mechanisms. J Neurosci 29:10387–10395

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gabriel JP, Ausborn J, Ampatzis K, Mahmood R, Eklof-Ljunggren E, El Manira A (2011) Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci 14:93–99

    CAS  PubMed  Google Scholar 

  • Huang Z, Satterlie RA (1990) Neuronal mechanisms underlying behavioral switching in a pteropod mollusk. J Comput Physiol A 166:875–887

    Google Scholar 

  • Katz PS, Fickbohm DJ, 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

    Google Scholar 

  • Kobzik L, Reid MB, Bredt DS, Stamler JS (1994) Nitric oxide in skeletal muscle. Nature 372:546–548

    CAS  PubMed  Google Scholar 

  • McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR (2008) Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 11:1419–1429

    CAS  PubMed  PubMed Central  Google Scholar 

  • McLean DL, Fetcho J (2009) Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones. J Neurosci 29:13566–13577

    CAS  PubMed  PubMed Central  Google Scholar 

  • McPherson DR, Blankenship JE (1991) Neural control of swimming in Aplysia brasiliana. III. Serotonergic modulatory neurons. J Neurophysiol 66:1366–1379

    CAS  PubMed  Google Scholar 

  • McPherson DR, Blankenship JE (1992) Neuronal modulation of foot and body-wall contractions in Aplysia californica. J Neurophysiol 67:23–28

    CAS  PubMed  Google Scholar 

  • Newcomb JM, Katz PS (2009) Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours. Proc R Soc London B 276:99–108

    Google Scholar 

  • Parsons DW, Pinsker HM (1988) Swimming in Aplysia brasiliana: identification of parapodial opener-phase and closer-phase neurons. J Neurophysiol 59:717–739

    CAS  PubMed  Google Scholar 

  • Parsons DW, Pinsker HM (1989) Swimming in Aplysia brasiliana: behavioral and cellular effects of serotonin. J Neurophysiol 62:1163–1176

    CAS  PubMed  Google Scholar 

  • Pirtle TJ, Satterlie RA (2006) The contribution of the pleural type 12 interneuron to swim acceleration in Clione limacina. Invert Neurosci 6:161–168

    PubMed  Google Scholar 

  • Satterlie RA (1993) Neuromuscular organization in the swimming system of the pteropod mollusc Clione limacina. J Exp Biol 181:119–140

    CAS  PubMed  Google Scholar 

  • Satterlie RA (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. II. Peripheral modulatory neurons. J Exp Biol 19:905–916

    Google Scholar 

  • Satterlie RA, Norekian TP (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. III. Cerebral neurons. J Exp Biol 198:917–930

    CAS  PubMed  Google Scholar 

  • Satterlie RA, Norekian TP (1997) Modulation of swimming speed in the pteropod mollusc, Clione limacina: role of a compartmental serotonergic system. Invert Neurosci 2:157–165

    Google Scholar 

  • Satterlie RA, Norekian TP (2001) Mechanisms of locomotory speed change: the pteropod solution. Am Zool 41:1001–1008

    Google Scholar 

  • Satterlie RA, Spencer AN (1985) Swimming in the pteropod mollusc, Clione limacina. II. Physiology. J Exp Biol 116:205–222

    Google Scholar 

  • Satterlie RA, LaBarbera M, Spencer AN (1985) Swimming in the pteropod mollusc, Clione limacina. I. Behaviour and Morphology. J Exp Biol 116:189–204

    Google Scholar 

  • Satterlie RA, Norekian TP, Jordan S, Kazilek CJ (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. I. Serotonin immunoreactivity in the central nervous system and wings. J Exp Biol 198:895–904

    CAS  PubMed  Google Scholar 

  • Satterlie RA, Norekian TP, Pirtle TJ (2000) Serotonin-induced spike narrowing in a locomotor pattern generator permits increases in cycle frequency during accelerations. J Neurophysiol 83:2163–2170

    CAS  PubMed  Google Scholar 

  • Song J, Pallucchi I, Ausborn J, Ampatzis K, Bertuzzi M, Fontanel P, Picton LD, El Manira A (2020) Multiple rhythm-generating circuits act in tandem with pacemaker properties to control the start and speed of locomotion. Neuron 105:1048–1061

    CAS  PubMed  Google Scholar 

  • Stamler JS, Meissner G (2001) Physiology of nitric oxide in skeletal muscle. Physiol Rev 81:209–237

    CAS  PubMed  Google Scholar 

  • Szymik BG, Satterlie RA (2011) Changes in the wingstroke kinematics associated with a change in swimming in a pteropod mollusk, Clione limacina. J Exp Biol 214:3935–3947

    PubMed  Google Scholar 

  • Szymik BG, Satterlie RA (2017) Circulation of hemocoelic fluid during slow and fast swimming in the pteropod mollusc Clione limacina. Invert Biol 136:290–300

    Google Scholar 

  • Wagner N (1885) Die Wirbellosen des Weissen Meeres: Zoologische Forschungen an der Kuste des Solowetzkischen Meerbusens in den Sommermonaten der Jahre 1877, 1878, 1879 und 1882. Verlag von Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Zhong G, Droho S, Crone SA, Dietz S, Kwan AC, Webb WW, Sharma K, Harris-Warrick RM (2010) Electrophysiological characterization of V2a interneurons and their locomotor-related activity in the neonatal mouse spinal cord. J Neurosci 30:170–182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong G, Sharma K, Harris-Warwick RM (2011) Frequency-dependent recruitment of V2a interneurons during fictive locomotion in mouse spinal cord. Nat Commun 2:274

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the staff and Director of Friday Harbor Laboratories, University of Washington, for providing laboratory space and support for this research, and the Honors College of the University of North Carolina Wilmington for support for J.B.P. Primary support for this project came from NSF grant IBN-9904424.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard A. Satterlie.

Ethics declarations

Conflict of interest

None.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Plyler, J.B., Satterlie, R.A. Pedal serotonergic neuron clusters of the pteropod mollusc, Clione limacina, contain two morphological subtypes with different innervation targets. Invert Neurosci 20, 21 (2020). https://doi.org/10.1007/s10158-020-00256-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10158-020-00256-0

Keywords

Navigation