Summary
In crustacean walking legs, the coxo-basipodite chordotonal organ (CB) composed of about 50 sensory cells, evokes a resistance reflex in the levator (Lev) and depressor (Dep) muscles responsible for the movements of the coxo-basipodite joint where it is located. Mechanical stimulation of the CB strand and electrical stimulation of its sensory nerve have been performed along with systematic intracellular recordings from CB terminals (CB T) and levator (Lev) or depressor (Dep) motoneurons (MNs) in order to study their connections. Measurements of conduction times in the CB nerve demonstrated different pools of sensory fibres, the fastest of which reach the ganglion in 2.5 ms. During imposed movements to the CB strand, intracellularly recorded Lev or Dep MN display EPSPs that are correlated to spikes in the CB nerve, their delays are incompatible with a polysynaptic pathway. Systematic stimulation of the CB nerve demonstrates that about 4 to 8 CB fibres are connected with each Lev or Dep MN. Classical tests for monosynaptic connections indicate that EPSPs occurring between 3 ms and 6 ms correspond mainly to monosynaptic connections with CB T, whereas IPSPs (the latencies of which are above 12 ms) are polysynaptic. In spite of the high selectivity of the CB T onto MNs, eight simultaneous intracellular recordings of coupled CB T and MN (out of more than 300 MNs penetrated) have allowed a direct measurement of synaptic delays (less than 1 ms). The functional significance of these results is discussed in relation to the proprioceptive control of locomotor movements.
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Abbreviations
- CB :
-
Coxo-basipodite chordotonal organ
- CB n :
-
CB sensory nerve
- CB T :
-
CB sensory terminal
- Dep :
-
depressor
- Lev :
-
levator
- MN :
-
motoneuron
References
Alexandrowicz JS (1957) Receptor elements in the coxal region of decapod Crustacea. J Mar Biol Ass UK 36:603–628
Ayers JL, Davis WJ (1977) Neuronal control of locomotion in the lobster, Homarus americanas. I. Motor programs for forward and backward walking. J Comp Physiol 115:1–27
Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: Brooks VB (ed) Handbook of physiology, Section I, The nervous system, motor control. American Physiological Society, Bethesda, MD, Vol. II, pp 509–595
Barnes WJP, Spirito LP, Evoy WH (1972) Nervous control of walking in the crab, Cardisoma guanhumi. II. Role of resistance reflexes in walking. J Comp Physiol 76:16–31
Bässler U, Büschges A (1990) Interneurones participating in the ‘active reaction’ in stick insects. Biol Cybern 62:529–538
Berry MS, Pentreath VW (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105:1–20
Blight AR, Llinás R (1980) The non-impulsive stretch-receptor complex of the crab — a study of depolarization-release coupling at a tonic sensorimotor synapse. Phil Trans R Soc Lond (Biol) 290:219–276
Buchanan JT, Grillner S, Cullheim S, Risling M (1989) Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology and function. J Neurophysiol 62:59–69
Burke W (1954) An organ for proprioception and vibration sense in Carcinus maenas. J Exp Biol 31:127–137
Burrows M (1975) Monosynaptic connexions between wing stretch receptors and flight motoneurones of the locust. J Exp Biol 62:189–219
Burrows M (1987) Parallel processing of proprioceptive signals by spiking local interneurons and motor neurons in the locust. J Neurosci 7:1064–1080
Büschges A (1990) Nonspiking pathways in a joint-control loop of the stick insect Carausius morosus. J Exp Biol 151:133–160
Bush BMH (1962) Proprioceptive reflexes in the legs of Carcinus maenas (L.). J Exp Biol 39:89–105
Bush BMH (1965a) Proprioception by the coxo-basal chordotonal organ, CB, in legs of the crab, Carcinus maenas. J Exp Biol 42:285–297
Bush BMH (1965b) Leg reflexes from chordotonal organs in the crab, Carcinus maenas. Comp Biochem Physiol 15:567–587
Cattaert D, El Manira A, Marchand A, Clarac F (1990) Central control of the sensory afferent terminals from a leg chordotonal organ in crayfish in vitro preparation. Neurosci Lett 108:81–87
Chrachri A, Clarac F (1989) Synaptic connections between motor neurons and interneurons in the fourth thoracic ganglion of the crayfish, Procambarus clarkii. J Neurophysiol 62:1237–1250
Clarac F (1985) Stepping reflexes and the sensory control of walking in Crustacea. In: Barnes WJP, Gladden MH (eds) Feedback and motor control in invertebrates and vertebrates. Croom Helm, London, pp 379–400
Clarac F, Vedel JP, Bush BMH (1978) Intersegmental reflex coordination by a single joint receptor organ (CB) in rock lobster walking legs. J Exp Biol 73:29–46
El Manira A, Cattaert D, Clarac F (1990a) Reflex reversal and presynaptic control of sensory afferents in Crustacea. Eur J Neurosci suppl 3:183
El Manira A, Cattaert D, Clarac F (1990b) GABAergic presynaptic inhibition as modulator of monosynaptic reflex in Crustacea. Soc Neurosci Abstr 16:1226
Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Brooks VB (ed) Handbook of physiology, Section I, The nervous system, motor control. American Physiological Society, Bethesda, MD, Vol. II, pp 1179–1236
Hartman HB, Boettiger EG (1967) The functional organization of the propus-dactylus organ in Cancer irroratus Say. Comp Biochem Physiol 22:651–663
Hasan Z, Stuart DG (1988) Animal solution to problems of movement control: the role of proprioceptors. Annu Rev Neurosci 11:199–223
Henneman E, Mendell LM (1981) Functional organization of motoneuron pool and its inputs. In: Brooks VB (ed) Handbook of physiology, The nervous system, motor control. American Physiological Society, Bethesda, MD, Section I, Vol. II, pp 423–507
Jahr CE, Yoshioka K (1985) Ia afferent excitation of motoneurons in the in vitro newborn rat spinal cord is selectively antagonized by kynurenate. J Physiol 370:515–530
Laurent G, Burrows M (1989a) Distribution of intersegmental inputs to nonspiking local interneurons and motor neurons in the locust. J Neurosci 9:3019–3029
Laurent G, Burrows M (1989b) Intersegmental interneurons can control the gain of reflexes in adjacent segments of the locust by their action on nonspiking local interneurons. J Neurosci 9:3030–3039
Mill PJ, Lowe DA (1973) The fine structure of the PD proprioceptor of Cancer pagurus. I. The receptor strand and the movement sensitive cells. Proc R Soc Lond B 184:179–197
Mill PJ (1976) Chordotonal organs of crustacean appendages. In: Mill PJ (ed) Structures and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 243–297
Reichert H, Krenz WD (1986) In vitro visualization of individual neurons in arthropod ganglia facilitates intracellular neuropil recording. J Comp Physiol A 158:625–637
Selverston A (1985) Model neural networks and behavior. Plenum Press, New York London
Sillar KT, Skorupski P (1986) Central input to primary afferent neurons in crayfish, Pacifastacus leniusculus, is correlated with rhythmic motor output of thoracic ganglia. J Neurophysiol 55:678–688
Skorupski P, Sillar KT (1986) Phase-dependent reversal of reflexes mediated by the thoracico-coxal muscle receptor organ in the crayfish, Pacifastacus leniusculus. J Neurophysiol 55:689–695
Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimidine tracer. Cell 17:741–759
Vedel JP (1982) Reflex reversal resulting from active movements in the antenna of the rock lobster. J Exp Biol 101:121–133
Whitear M (1962) The fine structure of crustacean proprioceptors. I. The chordotonal organs in the legs of the shore crab, Carcinus maenas. Phil Trans R Soc Lond B 245:291–325
Wiersma CAG (1959) Movement receptors in decapod Crustacea. J Mar Biol Ass UK 38:143–152
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El Manira, A., Cattaert, D. & Clarac, F. Monosynaptic connections mediate resistance reflex in crayfish (Procambarus clarkii) walking legs. J Comp Physiol A 168, 337–349 (1991). https://doi.org/10.1007/BF00198353
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DOI: https://doi.org/10.1007/BF00198353