Dorsal Root Potentials and Antidromic Discharges of Primary Afferents during Fictive Locomotion in the Cat

1. Cutaneous primary afferents were recorded intracellularly during fictive locomotion in decorticated cats with the goal of improving our understanding of how locomotor networks might centrally control the transmission in cutaneous pathways at a presynaptic level. 2. Identified cutaneous axons from superficialis peroneal nerve (SP) or tibialis posterior nerve (TP) were recorded intracellularly together with the electroneurograms (ENGs) of representative flexor and extensor muscle nerves of the hindlimb as well as dorsal root potential from L6 or L7 (DRP). Fictive locomotion occurred spontaneously after decortication (n = 12) or was induced by stimulation of the mesencephalic locomotor region (MLR) (n = 6). 3. The results revealed that all cutaneous axons (82 units with resting potential greater than 45 mV) showed fluctuations of their membrane potential (greater than or equal to 0.5 mV) at the rhythm of the fictive locomotion. The characteristics of fluctuation patterns, common to all cutaneous units, consisted of two depolarization waves per cycle: one related to the flexor activity, the other related to the extensor activity. The flexor-related depolarization was followed by a sharp trough of membrane repolarization. The extensor-related depolarization usually overlapped partly with the flexor-depolarization of the following cycle. The relative size of each depolarization could vary among different afferents of the same nerve in the same animal. Hence, maximal depolarization could occur in different parts of the locomotor cycle, but, for the majority of units (82%), it occurred during the flexor activity. These results were similar for SP and TP units. 4. Twenty percent of the units were discharging with a constant or irregular frequency. Phasic antidromic discharges related to locomotor ENGs were rarely encountered (5/82 units). 5. Linear regression analysis of the temporal relationships between fluctuations of membrane potential of cutaneous axons and locomotor bursts over several cycles showed that the timing of presynaptic events in cutaneous afferents is related to the events of the locomotor output. However, the same type of analysis showed that the amplitude of axonal depolarizations and the amplitude of flexor and extensor locomotor bursts could vary independently. Tight temporal relationships were also found between the depolarizations recorded in cutaneous units and the fluctuations recorded at the dorsal root level (DRP). 6. Based on the assumption that the locomotor fluctuations of cutaneous membrane potential are mediated through the primary afferent depolarization (PAD) pathways associated with presynaptic inhibition, it is proposed that the central pattern generator for locomotion (CPG) could phasically control the efficacy of transmission of cutaneous pathways at a presynaptic level as part of the locomotor program.

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Phase-dependent modulation of dorsal root potentials evoked by peripheral nerve stimulation during fictive locomotion in the cat

Brain Research ◽

10.1016/0006-8993(90)90333-7 ◽

1990 ◽

Vol 537 (1-2) ◽

pp. 1-13 ◽

Cited By ~ 33

Author(s):

Jean-Pierre Gossard ◽

Serge Rossignol

Keyword(s):

Peripheral Nerve ◽

Nerve Stimulation ◽

Dorsal Root ◽

Peripheral Nerve Stimulation ◽

Fictive Locomotion ◽

Dorsal Root Potentials

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Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat

Journal of Neurophysiology ◽

10.1152/jn.1988.60.6.2014 ◽

1988 ◽

Vol 60 (6) ◽

pp. 2014-2036 ◽

Cited By ~ 85

Author(s):

R. Dubuc ◽

J. M. Cabelguen ◽

S. Rossignol

Keyword(s):

Locomotor Activity ◽

Dorsal Root ◽

Primary Afferents ◽

Phase Point ◽

Fictive Locomotion ◽

Flexor Muscle ◽

Negative Wave ◽

Locomotor Rhythm ◽

Root Potential ◽

Point To Point

1. This study examines rhythmical activity of primary afferents occurring during "fictive" locomotion in decorticate paralyzed cats. Oscillations of the dorsal root potential (DRP) at the frequency of the locomotor rhythm have been observed at the lumbosacral and cervical levels. In addition, rhythmic antidromic discharges of primary afferent units have been recorded from the proximal stumps of cut dorsal root filaments. A detailed study of the relationships between the DRP fluctuations, the antidromic discharges, and the locomotor activity monitored by recording extensor and flexor muscle nerves is presented. 2. Typical DRP recordings from both lumbosacral and cervical levels show two negative waves (N1 and N2) separated by positive troughs (P1 and P2) in each locomotor cycle. Linear regression analyses indicate that the first negative wave (which generally has the largest amplitude) is related to the flexor activity whereas the second is related to the extensor activity. The relative amplitude of the two negative waves may vary without apparent concomitant changes in the recorded flexor or extensor motor nerves. The positive troughs occur respectively close to the period of transition between flexor and extensor activities and between extensor and flexor activities. 3. DRPs of similar period and amplitude can be observed in different ipsilateral roots recorded simultaneously. The DRPs recorded bilaterally from the same segment have the same periodicity but are out-of-phase. Point-to-point variations of amplitude in bilaterally recorded roots are not correlated. This suggests that the polarization of primary afferents on one side is mainly related to the locomotor events on that side. DRPs have been recorded in cats spinalized at Th13 and injected with nialamide and l-DOPA. This suggests that although the supraspinal contribution may be important, at least part of the DRPs may result from locomotor activity within the spinal cord itself. 4. A salient finding in our experiments was that of rhythmic antidromic unit discharges in the proximal stump of cut dorsal root filaments. Of the 194 units recorded, 19% (37/194) discharged in distinct bursts occurring at fixed times in the locomotor cycle. The majority of the units discharged either one burst during the period of flexor or extensor activity or one burst during one of the two periods of transition. Three units discharged two bursts per locomotor cycle. The frequency of the antidromic discharges of some units in one limb were also found to be modulated by stimulation of the skin or passive manipulation of the limbs.(ABSTRACT TRUNCATED AT 400 WORDS)

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Inhibition of Glutamatergic Synaptic Input to Spinal Lamina IIo Neurons by Presynaptic α2-Adrenergic Receptors

Journal of Neurophysiology ◽

10.1152/jn.00575.2001 ◽

2002 ◽

Vol 87 (4) ◽

pp. 1938-1947 ◽

Cited By ~ 86

Author(s):

Yu-Zhen Pan ◽

De-Pei Li ◽

Hui-Lin Pan

Keyword(s):

Receptor Antagonist ◽

Synaptic Input ◽

Adrenergic Receptors ◽

Adrenergic Receptor ◽

Dorsal Root ◽

Primary Afferents ◽

Noradrenergic System ◽

Analgesic Action ◽

Adrenergic Agonists ◽

Excitatory Synaptic Input

Activation of spinal α2-adrenergic receptors by the descending noradrenergic system and α2-adrenergic agonists produces analgesia. However, the sites and mechanisms of the analgesic action of spinally administered α2-adrenergic receptor agonists such as clonidine are not fully known. The dorsal horn neurons in the outer zone of lamina II (lamina IIo) are important for processing nociceptive information from C-fiber primary afferents. In the present study, we tested a hypothesis that activation of presynaptic α2-adrenergic receptors by clonidine inhibits the excitatory synaptic input to lamina IIo neurons. Whole cell voltage-clamp recordings were performed on visualized lamina IIo neurons in the spinal cord slice of rats. The miniature excitatory postsynaptic currents (mEPSCs) were recorded in the presence of tetrodotoxin, bicuculline, and strychnine. The evoked EPSCs were obtained by electrical stimulation of the dorsal root entry zone or the attached dorsal root. Both mEPSCs and evoked EPSCs were abolished by application of 6-cyano-7-nitroquinoxaline-2,3-dione. Clonidine (10 μM) significantly decreased the frequency of mEPSCs from 5.8 ± 0.9 to 2.7 ± 0.6 Hz (means ± SE) without altering the amplitude and the decay time constant of mEPSCs in 25 of 27 lamina IIo neurons. Yohimbine (2 μM, an α2-adrenergic receptor antagonist), but not prazosin (2 μM, an α1-adrenergic receptor antagonist), blocked the inhibitory effect of clonidine on the mEPSCs. Clonidine (1–20 μM, n = 8) also significantly attenuated the peak amplitude of evoked EPSCs in a concentration-dependent manner. The effect of clonidine on evoked EPSCs was abolished in the presence of yohimbine ( n = 5). These data suggest that clonidine inhibits the excitatory synaptic input to lamina IIo neurons through activation of α2-adrenergic receptors located on the glutamatergic afferent terminals. Presynaptic inhibition of glutamate release from primary afferents onto lamina IIoneurons likely plays an important role in the analgesic action produced by activation of the descending noradrenergic system and α2-adrenergic agonists.

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