In vivo analysis of proprioceptive coding and its antidromic modulation in the freely behaving crayfish.

Although sensory nerves in vitro are known to convey both orthodromic (sensory) and antidromic (putatively modulating) action potentials, in most cases very little is known about their bidirectional characteristics in intact animals. Here, we have investigated both the sensory coding properties and antidromic discharges that occur during real walking in the freely behaving crayfish. The activity of the sensory nerve innervating the proprioceptor CBCO, a chordotonal organ that monitors both angular movement and position of the coxo-basipodite (CB) joint, which is implicated in vertical leg movements, was recorded chronically along with the electromyographic activity of the muscles that control CB joint movements. Two wire electrodes placed on the sensory nerve were used to discriminate orthodromic from antidromic action potentials and thus allowed for analysis of both sensory coding and antidromic discharges. A distinction is proposed between 3 main classes of sensory neuron, according to their firing in relation to levator muscle activity during free walking. In parallel, we describe 2 types of antidromic activity: one produced exclusively during motor activity and a second produced both during and in the absence of motor activity. A negative correlation was found between the activity of sensory neurons in each of the 3 classes and identified antidromic discharges during walking. Finally, a state-dependent plasticity of CBCO nerve activity has been found by which the distribution of sensory orthodromic and antidromic activity changes with the physiological state of the biomechanical apparatus.

[1]  S. Rossignol,et al.  Intra-axonal recordings of cutaneous primary afferents during fictive locomotion in the cat. , 1989, Journal of neurophysiology.

[2]  Jean-Pierre Roll,et al.  Proprioceptive population coding of two-dimensional limb movements in humans: I. Muscle spindle feedback during spatially oriented movements , 2000, Experimental Brain Research.

[3]  S. Rossignol,et al.  Rhythmic antidromic discharges of single primary afferents recorded in cut dorsal root filaments during locomotion in the cat , 1985, Brain Research.

[4]  Daniel Cattaert,et al.  Effects of antidromic discharges in crayfish primary afferents. , 2002, Journal of neurophysiology.

[5]  F. Clarac,et al.  Functional analysis of the sensory motor pathway of resistance reflex in crayfish. I. Multisensory coding and motor neuron monosynaptic responses. , 1997, Journal of neurophysiology.

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

[7]  Presynaptic inhibition in the crayfish CNS: pathways and synaptic mechanisms. , 1985, Journal of neurophysiology.

[8]  F Clarac,et al.  Presynaptic inhibition is mediated by histamine and GABA in the crustacean escape reaction. , 1994, Journal of neurophysiology.

[9]  P. Harrison,et al.  Tidal wake-mixing localized effects on primary production and zooplankton distributions in the Strait of Georgia, British Columbia , 1992 .

[10]  S. Rossignol,et al.  An intracellular study of muscle primary afferents during fictive locomotion in the cat. , 1991, Journal of neurophysiology.

[11]  G. Loeb Hard lessons in motor control from the mammalian spinal cord , 1987, Trends in Neurosciences.

[12]  F. Clarac,et al.  Direct evidence for presynaptic inhibitory mechanisms in crayfish sensory afferents. , 1992, Journal of neurophysiology.

[13]  C. Bell,et al.  Primary afferent fibers conduct impulses in both directions under physiological stimulus conditions , 1985, Journal of Comparative Physiology A.

[14]  Domenici,et al.  Curve walking in freely moving crayfish (Procambarus clarkii) , 1998, The Journal of experimental biology.

[15]  E. Márquez A comparison of glutamic-oxalacetate transaminase, lactate dehydrogenase, alpha-hydroxybutyrate dehydrogenase, and creatine phosphokinase activities in non-spawning, pre-spawning, and spawning pink salmon. , 1976, Comparative biochemistry and physiology. B, Comparative biochemistry.

[16]  D G Stuart,et al.  Animal solutions to problems of movement control: the role of proprioceptors. , 1988, Annual review of neuroscience.

[17]  A. Marchand,et al.  Functional aspects of central electrical coupling in mechanoreceptor afferents of crayfish , 1994, Brain Research.

[18]  F. Clarac,et al.  Antidromic modulation of a proprioceptor sensory discharge in crayfish. , 1997, Journal of neurophysiology.

[19]  F. Clarac,et al.  Antidromic discharges of dorsal root afferents and inhibition of the lumbar monosynaptic reflex in the neonatal rat , 1999, Neuroscience.

[20]  J. Duysens,et al.  Load-regulating mechanisms in gait and posture: comparative aspects. , 2000, Physiological reviews.

[21]  A. Cannone,et al.  Sensory feedback and central afferent interaction in the muscle receptor organ of the crab, Carcinus maenas. , 1996, Journal of neurophysiology.

[22]  S. Rossignol,et al.  Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. , 1988, Journal of neurophysiology.

[23]  K. Westberg,et al.  Evidence for functional compartmentalization of trigeminal muscle spindle afferents during fictive mastication in the rabbit , 2000, The European journal of neuroscience.

[24]  Daniel Cattaert,et al.  Adaptive motor control in crayfish , 2001, Progress in Neurobiology.

[25]  Daniel Cattaert,et al.  Direct glutamate‐mediated presynaptic inhibition of sensory afferents by the postsynaptic motor neurons , 1998, The European journal of neuroscience.

[26]  J. Stephens,et al.  The reflex responses of single motor units in human first dorsal interosseous muscle following cutaneous afferent stimulation. , 1980, The Journal of physiology.

[27]  H. Hsiao,et al.  Miniature angle transducer for marine arthropods. , 1976, Comparative biochemistry and physiology. A, Comparative physiology.

[28]  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.

[29]  Daniel Cattaert,et al.  Efferent controls in crustacean mechanoreceptors , 2002, Microscopy research and technique.

[30]  P. Rudomín,et al.  Presynaptic modulation of spinal reflexes , 1993, Current Opinion in Neurobiology.

[31]  J. Gossard,et al.  Task-Dependent Presynaptic Inhibition , 2003, The Journal of Neuroscience.

[32]  P. Rudomín Selectivity of the central control of sensory information in the mammalian spinal cord. , 2002, Advances in experimental medicine and biology.

[33]  W. Barnes,et al.  Primary afferent depolarizations of sensory origin within contact-sensitive mechanoreceptive afferents of a crayfish leg. , 1997, Journal of neurophysiology.

[34]  A. Chrachri,et al.  Fictive locomotion in the fourth thoracic ganglion of the crayfish, Procambarus clarkii , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  D. Cattaert,et al.  Active Motor Neurons Potentiate Their Own Sensory Inputs via Glutamate-Induced Long-Term Potentiation , 1999, The Journal of Neuroscience.

[36]  S. Rossignol,et al.  Antidromic discharges in dorsal roots of decerebrate cats I. Studies at rest and during fictive locomotion , 1999, Brain Research.

[37]  F. Clarac,et al.  Antidromic discharges of dorsal root afferents in the neonatal rat , 1999, Journal of Physiology-Paris.

[38]  A. Manira,et al.  Presynaptic inhibition and antidromic discharges in crayfish primary afferents , 1999, Journal of Physiology-Paris.

[39]  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.

[40]  F. Clarac,et al.  Spontaneous and locomotor‐related GABAergic input onto primary afferents in the neonatal rat , 2000, The European journal of neuroscience.

[41]  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.

[42]  M. Göpfert,et al.  atonal is required for exoskeletal joint formation in the Drosophila auditory system , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[43]  STEERING REACTIONS AS ADAPTIVE COMPONENTS OF THE TAIL-FLIP IN THE SPINY LOBSTER JASUS LALANDII , 1992 .

[44]  S. Rossignol,et al.  The effects of antidromic discharges on orthodromic firing of primary afferents in the cat , 1999, Brain Research.

[45]  F. Clarac,et al.  Functional analysis of the sensory motor pathway of resistance reflex in crayfish. II. Integration Of sensory inputs in motor neurons. , 1997, Journal of neurophysiology.

[46]  S. Rossignol,et al.  Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. , 1988 .

[47]  W. Stein,et al.  Physiology of vibration-sensitive afferents in the femoral chordotonal organ of the stick insect , 1999, Journal of Comparative Physiology A.

[48]  Jamon,et al.  Locomotor patterns in freely moving crayfish (Procambarus clarkii) , 1995, The Journal of experimental biology.

[49]  J. Vedel,et al.  Recurrent Inhibition of Wrist Extensor Motoneurones: A Single Unit Study on a Deafferented Patient , 2003, The Journal of physiology.

[50]  D. McCrea Spinal circuitry of sensorimotor control of locomotion , 2001, The Journal of physiology.

[51]  F. Clarac,et al.  Influence of walking on swimmeret beating in the lobster Homarus gammarus. , 1983, Journal of neurobiology.

[52]  W D Willis,et al.  Depolarization of central terminals of Group I afferent fibres from muscle , 1962, The Journal of physiology.

[53]  Meta Virant-Doberlet,et al.  Communication with substrate-borne signals in small plant-dwelling insects. , 2003, Annual review of entomology.

[54]  P H Ellaway,et al.  Cumulative sum technique and its application to the analysis of peristimulus time histograms. , 1978, Electroencephalography and clinical neurophysiology.

[55]  G E Loeb,et al.  Monosynaptic and dorsal root reflexes during locomotion in normal and thalamic cats. , 1990, Journal of neurophysiology.

[56]  Jamon,et al.  Variability of leg kinematics in free-walking crayfish, Procambarus clarkii, and related inter-joint coordination , 1997, The Journal of experimental biology.