Skip to main content
SpringerLink
Log in

Rate modification in the heartbeat central pattern generator of the medicinal leech

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

  1. 1.

    Intracellular recordings from neurons in partially dissected leeches and isolated nerve cords were used to study the effects of temperature, sensory stimulation and locomotory activity on the output of the central pattern generator that drives heartbeat.

  2. 2.

    The rate of motor burst production by the heartbeat oscillator changes on gradual heating or cooling with a Q10 averaging around 2.4. Abrupt cooling of isolated nerve cords can induce additional changes in heart rate that are associated with ‘paradoxical’ firing of motor neurons.

  3. 3.

    Heart rate was accelerated when mechanical stimuli were applied to the body wall of partially dissected preparations or when restrained preparations spontaneously initiated movements. For instance, marked acceleration of heart rate occurred when preparations exhibited body movements and motor neuron activity characteristic of swimming in intact animals. Activation of the motor program for swimming in isolated nerve cords led to acceleration of heartbeat oscillator cycling. Accelerations of heart rate associated with swimming are therefore mediated at least partially through central interactions.

  4. 4.

    Individual identified neurons were tested for their influence on the cycle rate of the heartbeat oscillator in isolated nerve cords. Activity of individual mechanosensory neurons was found to accelerate heart rate. Touch mechanosensory neurons were also found to influence the heartbeat oscillator through a rapidly adapting inhibitory pathway. Activity of individual motorneurons generally did not affect heart rate. Some interneurons and neuroeffector cells known to cause motor activation (e.g. swim initiating interneurons, serotonergic Retzius cells) can also produce acceleration of heart rate.

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

Similar content being viewed by others

References

  • Arbas EA, Calabrese RL (1983) Leydig cell activity modulates heartbeat pattern generator cycling in the leech. Soc Neurosci Abstr 9:221.11

    Google Scholar 

  • Calabrese RL (1979) The roles of endogenous membrane properties and synaptic interaction in generating the heartbeat rhythm of the leech,Hirudo medicinalis. J Exp Biol 82:163–176

    Google Scholar 

  • Calabrese RL (1980) Control of multiple impulse-initiation sites in a leech interneuron. J Neurophysiol 44:878–896

    Google Scholar 

  • Calabrese RL, Peterson EL (1983) Neural control of heartbeat in the leech,Hirudo medicinalis. In: A Roberts, B Roberts (eds) Neural origin of rhythmic movements. Symp Soc Exp Biol 7:195–221

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

    Google Scholar 

  • Dickinson PS, Nagy F (1983) Control of a central pattern generator by an identified modulatory interneurone in Crustacea. II. Induction and modification of plateau properties in pyloric neurones. J Exp Biol 105:59–82

    Google Scholar 

  • Dieringer N, Koester J, Weiss KR (1978) Adaptive changes in heart rate ofAplysia californica. J Comp Physiol 123:11–21

    Google Scholar 

  • Frank E, Jansen JKS, Rinvik E (1975) A multisomatic axon in the central nervous system of the leech. J Comp Neurol 159:1–13

    Google Scholar 

  • Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex interactions. Physiol Rev 55:304–347

    Google Scholar 

  • Hartline DK (1979) Integrative neurophysiology of the lobster cardiac ganglion. Am Zool 19:53–65

    Google Scholar 

  • Kerkut GA, Taylor BJR (1956) Effect of temperature on the spontaneous activity from the isolated ganglia of the slug, cockroach and crayfish. Nature 178:426

    Google Scholar 

  • Keyser KT, Fraser BM, Lent CM (1982) Physiological and anatomical properties of Leydig cells in the segmental nervous system of the leech. J Comp Physiol 146:379–392

    Google Scholar 

  • Koch UT, Koester J (1982) Timesharing of heart power. J Comp Physiol 149:31–42

    Google Scholar 

  • Koester J, Dieringer N, Mandelbaum DE (1979) Cellular neuronal control of molluscan heart. Am Zool 19:103–116

    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, Calabrese RL (1976) Rhythmic swimming activity in neurons of the isolated nerve cord of the leech. J Exp Biol 65:643–668

    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 

  • Larimer J, Tindel JR (1966) Sensory modifications of heart rate in crayfish. Anim Behav 14:239–245

    Google Scholar 

  • Laverack MS (1961) The effect of temperature changes on the spontaneous nervous activity of the isolated nerve cord ofLumbricus terrestris. Comp Biochem Physiol 3:136–140

    Google Scholar 

  • Lippold OC, Nicholls JG, Redfearn JWT (1960) a study of the afferent discharge produced by cooling a mammalian muscle spindle. J Physiol 153:218–231

    Google Scholar 

  • Mann KH (1962) Leeches (Hirudinea). Pergamon Press, Oxford London New York

    Google Scholar 

  • Maranto AR, Calabrese RL (1984a) Neural control of the hearts in the leech,Hirudo medicinalis. I. Anatomy, electrical coupling and innervation of the hearts. J Comp Physiol A 154:367–380

    Google Scholar 

  • Maranto AR, Calabrese RL (1984b) Neural control of the hearts in the leech,Hirudo medicinalis. II. Myogenic activity and its control by heart motor neurons. J Comp Physiol A 154:381–391

    Google Scholar 

  • Mason A, Kristan WB Jr (1982) Neuronal excitation, inhibition and modulation of leech longitudinal muscle. J Comp Physiol 146:527–536

    Google Scholar 

  • Maynard D (1953) Activity in a crustacean ganglion. I. Cardioinhibition and acceleration inPanulirus argus. Biol Bull 104:156–170

    Google Scholar 

  • Miller JP, Selverston AI (1982a) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. II. Oscillatory properties of pyloric neurons. J Neurophysiol 48:1378–1391

    Google Scholar 

  • Miller JP, Selverston AI (1982b) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. IV. Network properties of pyloric system. J Neurophysiol 48:1416–1432

    Google Scholar 

  • Muller KJ, Nicholls JG, Stent GS (eds) (1981) Neurobiology of the leech. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Nagy F, Dickinson PS (1983) Control of a central pattern generator by an identified modulatory interneuron in Crustacea. I. Modulation of the pyloric motor output. J Exp Biol 105:33–58

    Google Scholar 

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

    Google Scholar 

  • Nicholls JG, Purves D (1970) Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J Physiol 209:647–667

    Google Scholar 

  • Ort CA, Kristan WB Jr, Stent GS (1974) Neuronal control of swimming in the medicinal leech. II. Identification and connection of neurons. J Comp Physiol 94:121–156

    Google Scholar 

  • Payton B (1981) Structure of the leech nervous system. In: Muller KJ, Nicholls JG, Stent GS (eds) Neurobiology of the leech. Cold Spring Harbor Laboratory Cold Spring Harbor, NY, pp 35–50

    Google Scholar 

  • Peterson EL (1983a) Generation and coordination of the heart-beat timing oscillation in the medicinal leech. I. Oscillatory neuronal circuits in isolated ganglia. J Neurophysiol 49:611–626

    Google Scholar 

  • Peterson EL (1983b) Generation and coordination of the heart-beat timing oscillator in the medicinal leech. II. The timer as a system of two coupled oscillators. J Neurophysiol 49:627–638

    Google Scholar 

  • Peterson EL, Calabrese RL (1982) Dynamic analysis of a rhythmic neural circuit in the leech,Hirudo medicinalis. J Neurophysiol 47:256–271

    Google Scholar 

  • Prosser CL (1973) Comparative animal physiology. W.B. Saunders Co, Philadelphia London

    Google Scholar 

  • Roberts BL, Roberts A (1983) Neural origins of rhythmic movements. Symp Soc Exp Biol 37

  • Sagawa K, Kumada M, Schramm LP (1974) Nervous control of the circulation. In: Guyton AC, Jones CE (eds) MTP International Review of Science, Physiology Series One, V/I Cardiovascular physiology. University Park Press, Baltimore, pp 197–232

    Google Scholar 

  • Selverston AI, Miller JP (1980) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. I. Pyloric system. J Neurophysiol 44:1102–1121

    Google Scholar 

  • Shafer M, Calabrese RL (1981) Similarities and differences in the structure of segmentally homologous neurons that control the hearts in the leech,Hirudo medicinalis. Cell Tissue Res 214:137–153

    Google Scholar 

  • Sigvardt KA, Mulloney B (1982) Sensory alteration of motor patterns in the stomatogastric nervous system of the spiny lobsterPanulirus interruptus. J Exp Biol 97:137–152

    Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. Freeman, San Francisco

    Google Scholar 

  • Stent GS, Thompson W, Calabrese RL (1978) Neuronal control of heartbeat in the leech and some other invertebrates. Physiol Rev 59:101–136

    Google Scholar 

  • Stuart AE (1970) Physiological and morphological properties of motoneurones in the central nervous system of the leech. J Physiol 209:627–646

    Google Scholar 

  • Thompson WJ, Stent GS (1976a) Neuronal control of heart-beat in the medicinal leech. I. Generation of the vascular constriction rhythm by heart motor neurons. J Comp Physiol 111:261–279

    Google Scholar 

  • Thompson WJ, Stent GS (1976b) Neuronal control of heart-beat in the medicinal leech. II. Intersegmental coordination of heart motor neuron activity by heart interneurons. J Comp Physiol 111:281–307

    Google Scholar 

  • Van Gelder N, Krnjevic K (1961) Sensitivity of crayfish stretch receptors to temperature changes. J Physiol 156:14–15

    Google Scholar 

  • Watson WH, Wyse GA (1978) Coordination of heart and gill rhythms inLimulus. J Comp Physiol 124:267–275

    Google Scholar 

  • Weeks JC (1982a) Segmental specialization of a leech swim-initiating interneuron, cell 205. J Neurosci 2:972–985

    Google Scholar 

  • Weeks JC (1982b) Synaptic basis of swim initiation in the leech I. Connections of a swim-initiating neuron (cell 204) with motor neurons and pattern-generating ‘oscillator’ neurons. J Comp Physiol 148:253–263

    Google Scholar 

  • Weeks JC (1982c) Synaptic basis of swim initiation in the leech. II. A pattern generating neuron (cell 208) which mediates motor effects of swim-initiating neurons. J Comp Physiol 148:265–279

    Google Scholar 

  • Weeks JC, Kristan WB Jr (1978) Initiation, maintenance, and modulation of swimming in the medicinal leech by activity of single neurone. J Exp Biol 77:71–88

    Google Scholar 

  • Willard AL (1981) Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J Neurosci 1:936–944

    Google Scholar 

  • Winter C (1973) The influence of temperature on membrane processes. In: Wieser W (ed) Effects of temperature on ectothermic organisms. Springer, Berlin Heidelberg New York pp 45–53

    Google Scholar 

  • Zebe E, Salge U, Wieman C, Wilps H (1981) The energy metabolism of the leechHirudo medicinalis in anoxia and muscular work. J Exp Zool 218:157–163

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biological Laboratories Harvard University, 16 Divinity Ave., 02138, Cambridge, Massachusetts, USA

    Edmund A. Arbas & Ronald L. Calabrese

Authors
  1. Edmund A. Arbas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ronald L. Calabrese
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arbas, E.A., Calabrese, R.L. Rate modification in the heartbeat central pattern generator of the medicinal leech. J. Comp. Physiol. 155, 783–794 (1984). https://doi.org/10.1007/BF00611595

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00611595

Keywords

Search

Navigation