State‐dependent regulation of sensory‐motor transmission: role of muscarinic receptors in sensory‐motor integration in the crayfish walking system

The aim of this study was to investigate a potential mechanism for state‐dependent regulation of sensory‐motor transmission from sensory afferents of a proprioceptor to motoneurons (MNs) in the walking system of the crayfish. This study was performed using an in vitro preparation of thoracic ganglia including motor nerves and the proprioceptor that codes movements of the second joint (coxo‐basal chordotonal organ − CBCO) of the leg. Application of movements to the CBCO elicits resistance reflex responses intracellularly recorded from Dep MNs. This reflex response is enhanced when Dep MNs are depolarized either spontaneously or by current injection. This enhancement is abolished in the presence of scopolamine (an antagonist of muscarinic acetylcholine receptors). Using pharmacology, we demonstrate that the monosynaptic connection from CBCO sensory neurons to the Dep MNs includes both nicotinic and muscarinic components. In addition, the shape of monosynaptic excitatory postsynaptic potentials (EPSPs) depends on the membrane potential: at a subthreshold depolarizing membrane potential, the time constant of the falling phase of the EPSPs is significantly increased compared with its value at resting potential. This change is suppressed in the presence of scopolamine, indicating that the muscarinic component may contribute to the activation of the Dep MN pool by sensory activity. This state‐dependent amplification of the sensory input may be important for increasing the strength of sensory feedback at times when central activation of the Dep MNs is very strong (e.g. during walking).

[1]  P. S. Dickinson,et al.  Control of a central pattern generator by an identified modulatory interneurone in crustacea. I. Modulation of the pyloric motor output. , 1983, The Journal of experimental biology.

[2]  M. Moulins,et al.  Sensory input induces long-lasting changes in the output of the lobster pyloric network. , 1990, Journal of neurophysiology.

[3]  R. Harris-Warrick,et al.  Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. , 1989, Journal of neurophysiology.

[4]  D. Livengood,et al.  Membrane current underlying muscarinic cholinergic excitation of motoneurons in lobster cardiac ganglion. , 1989, Journal of neurophysiology.

[5]  S. Komori,et al.  M2 and M3 muscarinic receptors couple, respectively, with activation of nonselective cationic channels and potassium channels in intestinal smooth muscle cells. , 1998, Japanese journal of pharmacology.

[6]  A. El Manira,et al.  Presynaptic Inhibition and Antidromic Spikes in Primary Afferents of the Crayfish: A Computational and Experimental Analysis , 2001, The Journal of Neuroscience.

[7]  A. Roberts,et al.  The stopping response of Xenopus laevis embryos: behaviour, development and physiology , 1992, Journal of Comparative Physiology A.

[8]  K. G. Pearson,et al.  Are there Central Pattern Generators for Walking and Flight in Insects , 1985 .

[9]  R. Dubuc,et al.  Role of sensory-evoked NMDA plateau potentials in the initiation of locomotion. , 1997, Science.

[10]  E Marder,et al.  Multiple Peptides Converge to Activate the Same Voltage-Dependent Current in a Central Pattern-Generating Circuit , 2000, The Journal of Neuroscience.

[11]  Örjan Ekeberg,et al.  A computer based model for realistic simulations of neural networks , 1991, Biological Cybernetics.

[12]  D. Cattaert,et al.  Inhibitory connections between antagonistic motor neurones of the crayfish walking legs , 1998, The Journal of comparative neurology.

[13]  E. Marder,et al.  The pharmacological properties of some crustacean neuronal acetylcholine, gamma‐aminobutyric acid, and L‐glutamate responses. , 1978, The Journal of physiology.

[14]  E. Florey Acetylcholine as sensory transmitter in crustacea , 1973, Journal of comparative physiology.

[15]  Daniel Cattaert,et al.  Peripheral Sensory Modules Controlling Motor Behavior , 2000 .

[16]  E. Kravitz,et al.  Acetylcholine and lobster sensory neurones , 1972, The Journal of physiology.

[17]  E. Kravitz,et al.  DISTRIBUTION OF ACETYLCHOLINE, CHOLINE, CHOLINE ACETYLTRANSFERASE AND ACETYLCHOLINESTERASE IN REGIONS AND SINGLE IDENTIFIED AXONS OF THE LOBSTER NERVOUS SYSTEM , 1974, Journal of neurochemistry.

[18]  M. P. Nusbaum,et al.  Long-lasting activation of rhythmic neuronal activity by a novel mechanosensory system in the crustacean stomatogastric nervous system. , 2004, Journal of neurophysiology.

[19]  P. Meyrand,et al.  Dynamic Restructuring of a Rhythmic Motor Program by a Single Mechanoreceptor Neuron in Lobster , 1999, The Journal of Neuroscience.

[20]  B. Mulloney,et al.  Sensory alteration of motor patterns in the stomatogastric nervous system of the spiny lobster Panulirus interruptus. , 1982, The Journal of experimental biology.

[21]  R. Dubuc,et al.  A Cellular Mechanism for the Transformation of a Sensory Input into a Motor Command , 2000, The Journal of Neuroscience.

[22]  P. Simmons,et al.  Cytochemical evidence that acetylcholine is a neurotransmitter of neurons that make excitatory and inhibitory outputs in the locust ocellar visual system , 2000, The Journal of comparative neurology.

[23]  B Mulloney,et al.  Cholinergic modulation of the swimmeret motor system in crayfish. , 1993, Journal of neurophysiology.

[24]  K. Sillar,et al.  Central input to primary afferent neurons in crayfish, Pacifastacus leniusculus, is correlated with rhythmic motor output of thoracic ganglia. , 1986, Journal of neurophysiology.

[25]  S. Anderson,et al.  Muscarinic acetylcholine receptor compounds alter net Ca2+ flux and contractility in an invertebrate smooth muscle , 2003, Invertebrate Neuroscience.

[26]  Daniel Cattaert,et al.  Serotonin Enhances the Resistance Reflex of the Locomotor Network of the Crayfish through Multiple Modulatory Effects that Act Cooperatively , 2004, The Journal of Neuroscience.

[27]  B. Trimmer,et al.  Muscarinic acetylcholine receptors modulate the excitability of an identified insect motoneuron. , 1993, Journal of Neurophysiology.

[28]  T. Bolton,et al.  Muscarinic cation current and suppression of Ca2+ current in guinea pig ileal smooth muscle cells. , 1998, European journal of pharmacology.

[29]  D. Cattaert,et al.  Neural mechanisms of reflex reversal in coxo-basipodite depressor motor neurons of the crayfish. , 1997, Journal of neurophysiology.

[30]  U. Homberg Neurotransmitters and neuropeptides in the brain of the locust , 2002, Microscopy research and technique.

[31]  S. Grillner,et al.  Neuronal network generating locomotor behavior in lamprey: circuitry, transmitters, membrane properties, and simulation. , 1991, Annual review of neuroscience.

[32]  M. S. Berry,et al.  Criteria for distinguishing between monosynaptic and polysynaptic transmission , 1976, Brain Research.

[33]  Cholinergic transmission at the first synapse of the circuit mediating the crayfish lateral giant escape reaction. , 1992, Journal of neurophysiology.

[34]  A. Roberts,et al.  Sensory Activation and Role of Inhibitory Reticulospinal Neurons that Stop Swimming in Hatchling Frog Tadpoles , 2002, The Journal of Neuroscience.

[35]  F. Clarac,et al.  Cholinergic control of the walking network in the crayfish Procambarus clarkii , 1995, Journal of Physiology-Paris.

[36]  F. Clarac,et al.  Monosynaptic connections mediate resistance reflex in crayfish (Procambarus clarkii) walking legs , 1991, Journal of Comparative Physiology A.

[37]  A. Selverston,et al.  Mechanisms of gastric rhythm generation in the isolated stomatogastric ganglion of spiny lobsters: bursting pacemaker potentials, synaptic interactions, and muscarinic modulation. , 1992, Journal of neurophysiology.

[38]  D. Cattaert,et al.  Inhibitory component of the resistance reflex in the locomotor network of the crayfish. , 2002, Journal of neurophysiology.

[39]  M. Moulins,et al.  Muscarinic modulation of a pattern-generating network: control of neuronal properties , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  G. Mpitsos,et al.  Characterization of Muscarinic Cholinergic Receptors in the Crab Nervous System , 1986, Journal of neurochemistry.

[41]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[42]  W Buño,et al.  Nicotinic and muscarinic activation of motoneurons in the crayfish locomotor network. , 1994, Journal of neurophysiology.

[43]  Barry A. Trimmer,et al.  Current excitement from insect muscarinic receptors , 1995, Trends in Neurosciences.