Effects of antidromic discharges in crayfish primary afferents.

Contrary to orthodromic spikes that are generated in sensory organs and conveyed to CNS, antidromic spikes are generated in the axon terminals of the sensory neurons within the CNS and are conveyed to the peripheral sensory organ. Antidromic discharges are observed in primary afferent neurons of both vertebrates and invertebrates and seem to be related to the rhythmic activity of central neural networks. In this study, we analyzed the effect of antidromic discharges on the sensory activity of a leg proprioceptor in in vitro preparations of the crayfish CNS. Intracellular microelectrodes were used both to record the orthodromic spikes and to elicit antidromic spikes by injecting squares pulses of depolarizing current at various frequencies. Experiments were performed on the three types of identified sensory afferents (tonic, phasotonic, and phasic). The main results showed a reduction of the firing frequency of the orthodromic activity in 82% of the tested afferents. In tonic afferents, during their occurrences and according to their frequency, antidromic spikes or bursts reduced or suppressed the orthodromic activity. Following their terminations, they also induced a silent period and a gradual recovery of the orthodromic activity, both of which increased as the duration and the frequency of the antidromic bursts increased. In phasotonic and phasic afferents, antidromic bursts reduced or suppressed the phasic responses as their frequency and durations increased. In phasotonic afferents, if elicited prior to the movements, long-duration bursts with increasing frequency reduced more rapidly the tonic background activity than the phasic one whereas short-duration bursts at high frequency produced strong decreases of both. The effect of antidromic bursts accumulated when they are repetitively elicited. Antidromic bursts induced a much larger decrease of the sensory activity than adaptation alone. The occurrences of antidromic spikes or bursts may have a functional role in modulating the incoming sensory messages during locomotion. The mechanisms by which antidromic spikes modulate the firing sensitivity of the primary afferents may well lie in modifications of the properties of either mecanotransduction and/or spike initiation.

[1]  U. Bässler.  Afferent control of walking movements in the stick insectCuniculina impigra , 1986, Journal of Comparative Physiology A.

[2]  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.

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

[4]  Presynaptic inhibition of exteroceptive afferents by proprioceptive afferents in the terminal abdominal ganglion of the crayfish. , 1996, Journal of neurophysiology.

[5]  R. Calabrese,et al.  Presynaptic Inhibition: Primary Afferent Depolarization in Crayfish Neurons , 1974, Science.

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

[7]  J. Ochoa,et al.  Dorsal root reflexes , 1995 .

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

[9]  E. Anderson,et al.  Non-GABA mediated primary afferent depolarization , 1976, Brain Research.

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

[11]  Daniel Cattaert,et al.  Chloride conductance produces both presynaptic inhibition and antidromic spikes in primary afferents , 1994, Brain Research.

[12]  Daniel Cattaert,et al.  Shunting versus Inactivation: Analysis of Presynaptic Inhibitory Mechanisms in Primary Afferents of the Crayfish , 1999, The Journal of Neuroscience.

[13]  F. Cerveró,et al.  Mechanisms of touch-evoked pain (allodynia): a new model , 1996, Pain.

[14]  W. Willis Jr.  Dorsal root potentials and dorsal root reflexes: a double-edged sword , 1999 .

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

[16]  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.

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

[18]  G. A. Kerkut,et al.  An investigation of the dorsal root reflex using an in vitro preparation of the hamster spinal cord , 1985, Brain Research.

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

[20]  F. Clarac,et al.  Monosynaptic Interjoint Reflexes and their Central Modulation During Fictive Locomotion in Crayfish , 1991, The European journal of neuroscience.

[21]  J. Wine,et al.  Identified interneurons produce both primary afferent depolarization and presynaptic inhibition. , 1984, Science.

[22]  Can antidromic stimulation of rat muscle afferents modulate the sensitivity of muscle spindles? , 1998, Neuroscience Letters.

[23]  F. Clarac,et al.  Reversal of a Walking Leg Reflex Elicited by a Muscle Receptor , 1981 .

[24]  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.

[25]  J. Gossard.  Control of transmission in muscle group IA afferents during fictive locomotion in the cat. , 1996, Journal of neurophysiology.

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

[27]  K. Pearson.  REFLEX REVERSAL IN THE WALKING SYSTEMS OF MAMMALS AND ARTHROPODS , 1995 .

[28]  J. F. Yang,et al.  Mechanism for reflex reversal during walking in human tibialis anterior muscle revealed by single motor unit recording. , 1995, The Journal of physiology.

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

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

[31]  P. Rudomin,et al.  PAD patterns of physiologically identified afferent fibres from the medial gastrocnemius muscle , 2004, Experimental Brain Research.

[32]  K. Sillar,et al.  Phase-dependent reversal of reflexes mediated by the thoracocoxal muscle receptor organ in the crayfish, Pacifastacus leniusculus. , 1986, Journal of neurophysiology.

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

[34]  G. Pethő,et al.  Spike generation from dorsal roots and cutaneous afferents by hypoxia or hypercapnia in the rat in vivo , 1999, Experimental physiology.

[35]  J. Duysens,et al.  Gating and reversal of reflexes in ankle muscles during human walking , 2004, Experimental Brain Research.

[36]  B Hedwig,et al.  Presynaptic inhibition of sensory neurons during kicking movements in the locust. , 1996, Journal of neurophysiology.

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

[38]  J. Vedel,et al.  Reflex Reversal Resulting From Active Movements in the Antenna of the Rock Lobster , 1982 .

[39]  J. Eccles,et al.  Pharmacological studies on presynaptic inhibition , 1963, The Journal of physiology.

[40]  Presynaptic inhibition of transmission from identified interneurons in locust central nervous system. , 1981, Journal of neurophysiology.

[41]  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.

[42]  John C. Eccles,et al.  THE MODE OF OPERATION OF THE SYNAPTIC MECHANISM PRODUCING PRESYNAPTIC INHIBITION , 1963 .

[43]  J. Bagust,et al.  Correlation between spontaneous bursts of activity recorded from the dorsal roots in an isolated hamster spinal cord preparation , 1993, Experimental physiology.

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

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

[46]  P. Kostyuk,et al.  Polarization of primary afferent terminals of lumbosacral cord elicited by the activity of spinal locomotor generator , 1982, Neuroscience.

[47]  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.

[48]  J. Bagust,et al.  ToxinI, but not 4-aminopyridine, blocks the late inhibitory component of the dorsal root reflex in an isolated preparation of rat spinal cord , 1997, Brain Research.