Peripheral proprioceptive modulation in crayfish walking leg by serotonin

In vitro serotoninergic modulation of intracellularly recorded sensory responses was examined in primary afferent terminals of a crayfish leg proprioceptor, the coxo-basal chordotonal organ (CB CO). The effects of different concentrations of serotonin (5-HT) on static and dynamic sensory responses were analysed following bath or pressure applications of the monoamine directly on the strand of the mechanoreceptor. Consequently, the reported effects result from the direct peripheral action of 5-HT on the sensory organ itself. Serotonin modulates the sensory activity by modifying the sensory discharge frequency. The firing discharge of the primary afferents is increased in a dose-dependent manner. The maximal effect is obtained with a concentration of 10(-6) M. Higher concentrations are less effective, and for 20% of the recorded cells, 10(-4) M 5-HT induces a decrease of the sensory discharge, i.e. has an inhibitory effect. Alteration in the pattern of sensory firing, resulting in bursting discharge, was observed in some units. All the recorded sensory units were responsive to the neuromodulator whatever their functional properties. The effects of 5-HT lasted as long as the amine was applied and were reversible after wash. The results suggest that 5-HT could exert a modulatory action on the proprioceptive feedback, by peripheral action on the sensory organ. The natural modalities of 5-HT action are discussed on the basis of immunohistochemistry data suggesting: (i) connections between CB CO and central serotoninergic cells, (ii) 5-HT content in sensory cells of the CB CO. Since the CB CO is involved in the control of leg movement and position, the modulation of its primary afferents might influence the organization of the locomotor pattern. The functional significance of this peripheral sensory neuromodulation was approached by the analysis of the motor reflex activity.

[1]  I. Cooke,et al.  6 – Hormones and Neurosecretion , 1982 .

[2]  R. A. Davidoff,et al.  An in vitro study of the effects of serotonin on frog primary afferent terminals , 1990, Neuroscience Letters.

[3]  O. Kiehn,et al.  Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. , 1988, The Journal of physiology.

[4]  N. Tyrer,et al.  Immunohistochemical localization of serotonin and choline acetyltransferase in sensory neurones of the locust , 1988, The Journal of comparative neurology.

[5]  R. Harris-Warrick,et al.  Modulation of neural networks for behavior. , 1991, Annual review of neuroscience.

[6]  F. Krasne,et al.  Serotonin and octopamine have opposite modulatory effects on the crayfish's lateral giant escape reaction , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  OCTOPAMINERGIC MODULATION OF THE FOREWING STRETCH RECEPTOR IN THE LOCUST LOCUSTA MIGRATORIA , 1990 .

[8]  Stretch-induced release of proctolin from the dendrites of a lobster sense organ , 1988, Brain Research.

[9]  R. Elofsson,et al.  Identification and quantitative measurements of biogenic amines and DOPA in the central nervous system and haemolymph of the crayfish Pacif ast acus leniusculus (crustacea) , 1982 .

[10]  Randolf Menzel,et al.  Chemical codes for the control of behaviour in arthropods , 1989, Nature.

[11]  B. Bush,et al.  Primary afferent responses of a crustacean mechanoreceptor are modulated by proctolin, octopamine, and serotonin. , 1989, Journal of neurobiology.

[12]  Mapping of serotonin-like immunoreactivity in the ventral nerve cord of crayfish , 1990, Brain Research.

[13]  D. Maynard,et al.  Neurohormones of the pericardial organs of brachyuran Crustacea , 1959, The Journal of physiology.

[14]  E. Kravitz,et al.  The action of serotonin on excitatory nerve terminals in lobster nerve‐muscle preparations. , 1982, The Journal of physiology.

[15]  R. Harris-Warrick,et al.  Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord. , 1985, The Journal of experimental biology.

[16]  E. Kravitz,et al.  Mapping of serotonin-like immunoreactivity in the lobster nervous system , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  E R Kandel,et al.  Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  E. Florey,et al.  The effects of octopamine and other amines on the heart and on neuromuscular transmission in decapod crustaceans: further evidence for a role as neurohormone. , 1978, Comparative biochemistry and physiology. C: Comparative pharmacology.

[19]  R. Harris-Warrick,et al.  Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. , 1989, Journal of neurophysiology.

[20]  R. Harris-Warrick,et al.  Neurohormones and lobsters: biochemistry to behavior , 1983, Trends in Neurosciences.

[21]  F. Clarac,et al.  Intersegmental Coordination of Central Neural Oscillators for Rhythmic Movements of the Walking Legs in Crayfish, Pacifastacus Leniusculus , 1987 .

[22]  B. Bush,et al.  Peripheral modulation of mechanosensitivity in primary afferent neurons , 1987, Nature.

[23]  A. Chrachri,et al.  Synaptic connections between motor neurons and interneurons in the fourth thoracic ganglion of the crayfish, Procambarus clarkii. , 1989, Journal of neurophysiology.

[24]  D E Claassen,et al.  Effects of octopamine, dopamine, and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. , 1986, Journal of neurobiology.

[25]  H. Wigström,et al.  Maintained changes in motoneuronal excitability by short‐lasting synaptic inputs in the decerebrate cat. , 1988, The Journal of physiology.

[26]  L. Fischer,et al.  Octopamine action on the contractile system of crustacean skeletal muscle. , 1987, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[27]  D. Bliss The Biology of Crustacea , 1982 .

[28]  R. Harris-Warrick,et al.  Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  R. Sandeman,et al.  Atlas of serotonin‐containing neurons in the optic lobes and brain of the crayfish, Cherax destructor , 1988, The Journal of comparative neurology.

[30]  R. Harris-Warrick,et al.  Amines and a peptide as neurohormones in lobsters: actions on neuromuscular preparations and preliminary behavioural studies. , 1980, The Journal of experimental biology.

[31]  A. El Manira,et al.  Serotonin and proctolin modulate the response of a stretch receptor in crayfish , 1991, Brain Research.

[32]  H. Atwood,et al.  Pericardial peptides enhance synaptic transmission and tension in phasic extensor muscles of crayfish , 1990, Neuroscience Letters.

[33]  J. Wilkens,et al.  Dopamine and nicotine, but not serotonin, modulate the crustacean ventilatory pattern generator. , 1992, Journal of neurobiology.

[34]  T. Carew,et al.  Locomotion in Aplysia: triggering by serotonin and modulation by bag cell extract , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  N. Dun,et al.  5‐Hydroxytryptamine responses in neonate rat motoneurones in vitro. , 1990, The Journal of physiology.

[36]  A. L. Willard,et al.  Effects of serotonin on the generation of the motor program for swimming by the medicinal leech , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  E. Kravitz,et al.  Physiological identification, morphological analysis, and development of identified serotonin-proctolin containing neurons in the lobster ventral nerve cord , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  L. Fischer,et al.  Modulation of synaptic transmission and excitation-contraction coupling in the opener muscle of the crayfish, Astacus leptodactylus, by 5-hydroxytryptamine and octopamine. , 1983, The Journal of experimental biology.

[39]  S. Arnesen,et al.  The effects of serotonin and octopamine on behavioral arousal in the crayfish , 1988 .

[40]  E. Kravitz Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. , 1988, Science.

[41]  H. Pinsker,et al.  Swimming in Aplysia brasiliana: behavioral and cellular effects of serotonin. , 1989, Journal of neurophysiology.

[42]  M. Livingstone,et al.  Biochemistry and ultrastructure of serotonergic nerve endings in the lobster: serotonin and octopamine are contained in different nerve endings. , 1981, Journal of neurobiology.

[43]  E. Kravitz,et al.  Serotonin-containing neurons in lobsters: their role as gain-setters in postural control mechanisms. , 1992, Journal of neurophysiology.

[44]  R. Harris-Warrick,et al.  Serotonin and Octopamine Produce Opposite Postures in Lobsters , 1980, Science.