A kinematic study of crawling behavior in the leech,Hirudo medicinalis
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The medicinal leech crawls along a solid substrate by repeated alternating extensions and shortenings of the body. Extension occurs with the posterior sucker attached and the head sucker free. The head sucker then attaches, followed by shortening and release of the tail sucker. The tail sucker is then pulled toward the head, where it reattaches to the substrate. The head sucker then releases, and another crawling cycle begins (Figs. 1, 5).
There are two crawling variants: inchworm crawling, in which the head and tail suckers are closely apposed at the end of a cycle and the body forms a loop above the substrate, and vermiform crawling, in which the suckers are placed farther apart and the body remains fairly close to the substrate (Fig. 1).
The cycle period and the distance traveled during a cycle are greater in inchworm than in vermiform crawling; however, the velocity of travel is the same for both (Fig. 2).
For both variants, the interval between head sucker attachment and tail sucker release is similar at all cycle periods and has a value consistent with direct interneuronal conduction of a signal from head sucker sensory neurons to tail sucker motor neurons. The interval between tail sucker attachment and head sucker release, however, is longer and varies with the cycle period, suggesting a more complex interneuronal circuit in the pathway from tail sucker sensory neurons to head sucker motor neurons (Fig. 4).
The onsets of the components of the crawling cycle (extension, post-extension pause, shortening, and post-shortening pause) show an anteroposterior lag (Figs. 5, 7). For both variants, the travel time between segments varies directly with the period (Fig. 8).
For both crawl types, the durations of the cycle components vary directly with the period, with several exceptions (Figs. 9, 10).
A model is presented that summarizes the coordination of the various motor events in a cycle of leech crawling (Figs. 11 and 12).
KeywordsTravel Time Motor Neuron Sensory Neuron Solid Substrate Cycle Period
intersegmental travel time
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- Bowerman RF (1975) The control of walking in the scorpion. I. Leg movements during normal walking. J Comp Physiol 100:183–196Google Scholar
- Brodfeuhrer PD, Friesen WO (1984) A sensory system initiating swimming activity in the medicinal leech. J Exp Biol 108:341–355Google Scholar
- Burns MD (1973) The control of walking in Orthoptera. I. Leg movements in normal walking. J Exp Biol 58:45–58Google Scholar
- Burrows M, Willows AOD (1969) Neural coordination of rhythmic maxillipede beating in branchyuran and anomuran Crustacea. Comp Biochem Physiol 31:121–135Google Scholar
- Cattaert D, Clarac F (1983) Influence of walking on swimmeret beating in the lobster,Homarus gammarus. J Neurobiol 14:421–439Google Scholar
- Cohen AH, Holmes PJ, Rand RH (1982) The nature of coupling between segmental oscillators of the lamprey spinal generator for locomotion: a mathematical model. J Math Biol 13:345–369Google Scholar
- Davis WJ, Mpitsos GM, Pinneo JM (1974a) Modification of the behavioral hierarchy ofPleurobranchaea. I. The dominant position of the feeding behavior. J Comp Physiol 90:207–224Google Scholar
- Davis WJ, Mpitsos GM, Pinneo JM (1974b) Modification of the behavioral hierarchy ofPleurobranchaea. II. Hormonal suppression of feeding associated with egg-laying. J Comp Physiol 90:225–243Google Scholar
- Friesen WO, Poon M, Stent GS (1978) Neuronal control of swimming in the medicinal leech. IV. Identification of a network of oscillatory neurons. J Exp Biol 75:25–43Google Scholar
- Gray J, Lissman HW, Pumphrey RJ (1938) The mechanism of locomotion in the leech (Hirudo medicinalis). J Exp Biol 15:408–430Google Scholar
- Grillner S (1974) On the generation of locomotion in the spinal dogfish. Exp Brain Res 20:459–470Google Scholar
- Hening WA, Walters ET, Carew TJ, Kandel ER (1979) Motoneuronal control of locomotion inAplysia. Brain Res 179:231–253Google Scholar
- Kristan WB Jr, Stent GS, Ort CA (1974) Neuronal control of swimming in the medicinal leech. I. Dynamics of the swimming rhythm. J Comp Physiol 94:97–119Google Scholar
- Lent CM, Dickinson MH (1984) Serotonin integrates the feeding behavior of the medicinal leech. J Comp Physiol A154:457–471Google Scholar
- Mackey S, Carew TJ (1983) Locomotion inAplysia: triggering by serotonin and modulation by bag cell extract. J Neurosci 3:1469–1477Google Scholar
- Nusbaum M (1986) Swim initiation in the leech by serotonincontaining interneurons cells 21 and 61. J Exp Biol, in pressGoogle Scholar
- Ort CA, Kristan WB Jr, Stent GS (1974) Neural control of swimming in the medicinal leech. II. Physiological and morphological properties of motoneurons in the central nervous system of the leech. J Comp Physiol 94:121–154Google Scholar
- Pearson KG (1972) Central programming and reflex control of walking in the cockroach. J Exp Biol 56:173–193Google Scholar
- Pearson KG, Iles JF (1970) Discharge patterns of coxal levator and depressor motoneurons in the cockroach,Periplaneta americana. J Exp Biol 52:139–165Google Scholar
- Sawyer RT (1981) Leech biology and behavior. In: Muller K et al. (eds) Neurobiology of the leech. Cold Spring Harbor, pp 3–26Google Scholar
- Snedecor GW, Cochran WO (1967) Statistical methods, 6th edn. Iowa University PressGoogle Scholar
- Stein PSG (1971) Intersegmental coordination of swimmeret motoneuron activity in crayfish. J Neurophysiol 34:310–318Google Scholar
- Stern-Tomlinson W, Nusbaum MP, Kristan WB Jr (1984) Crawling in the leech. Soc Neurosci Abstr 10:396Google Scholar
- Stern-Tomlinson W, Nusbaum MP, Perez LE, Kristan WB Jr (1985) A quantitative study of the variants of crawling in the leech. Soc Neurosci Abstr 11:267Google Scholar
- Thompson WJ, Stent GS (1976) Neuronal control of heartbeat in the medicinal leech. II. Intersegmental coordination of heart motor neuron activity by heart interneurons. J Comp Physiol: 111, 281–307Google Scholar
- Trueman ER (1975) The locomotion of soft-bodied animals. American Elsevier, pp 16–41Google Scholar
- Weeks JC (1981) Neuronal basis of leech swimming: separation of swim initiation, pattern generation, and intersegmental coordination by selective lesions. J Neurophysiol 45:698–723Google Scholar
- Weeks JC (1982a) 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 148:253–263Google Scholar
- Weeks JC (1982b) 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 148:265–279Google Scholar
- Weeks JC, Kristan WB Jr (1978) Initiation, maintenance, and modulation of swimming in the leech by the activity of a single neurone. J Exp Biol 77:71–88Google Scholar
- Willard A (1981) Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J Neurosci 1:936–944Google Scholar