Sensory Integration in Presynaptic Inhibitory Pathways During Fictive Locomotion in the Cat

2002 ◽  
Vol 88 (1) ◽  
pp. 163-171 ◽  
Author(s):  
Ariane Ménard ◽  
Hugues Leblond ◽  
Jean-Pierre Gossard
Keyword(s):  
Presynaptic Inhibition ◽  
Muscle Afferents ◽  
Primary Afferent Depolarization ◽  
Skin Area ◽  
Fictive Locomotion ◽  
Step Cycle ◽  
Primary Afferent ◽  
Decerebrate Cat ◽  
Group I ◽  
Group I Afferents

The aim of this study is to understand how sensory inputs of different modalities are integrated into spinal cord pathways controlling presynaptic inhibition during locomotion. Primary afferent depolarization (PAD), an estimate of presynaptic inhibition, was recorded intra-axonally in group I afferents ( n = 31) from seven hindlimb muscles in L6–S1 segments during fictive locomotion in the decerebrate cat. PADs were evoked by stimulating alternatively low-threshold afferents from a flexor nerve, a cutaneous nerve and a combination of both. The fictive step cycle was divided in five bins and PADs were averaged in each bin and their amplitude compared. PADs evoked by muscle stimuli alone showed a significant phase-dependent modulation in 20/31 group I afferents. In 12/20 afferents, the cutaneous stimuli alone evoked a phase-dependent modulation of primary afferent hyperpolarization (PAH, n = 9) or of PADs ( n = 3). Combining the two sensory modalities showed that cutaneous volleys could significantly modify the amplitude of PADs evoked by muscle stimuli in at least one part (bin) of the step cycle in 17/31 (55%) of group I afferents. The most common effect (13/17) was a decrease in the PAD amplitude by 35% on average, whereas it was increased by 17% on average in the others (4/17). Moreover, in 8/13 afferents, the PAD reduction was obtained in 4/5 bins i.e., for most of the duration of the step cycle. These effects were seen in group I afferents from all seven muscles. On the other hand, we found that different cutaneous nerves had quite different efficacy; the superficial peroneal (SP) being the most efficient (85% of trials) followed by Saphenous (60%) and caudal sural (44%) nerves. The results indicate that cutaneous interneurons may act, in part, by modulating the transmission in PAD pathways activated by group I muscle afferents. We conclude that cutaneous input, especially from the skin area on the dorsum of the paw (SP), could subtract presynaptic inhibition in some group I afferents during perturbations of stepping (e.g., hitting an obstacle) and could thus adjust the influence of proprioceptive feedback onto motoneuronal excitability.

Convergence onto interneurons subserving primary afferent depolarization of group I afferents

1984 ◽  
Vol 51 (3) ◽  
pp. 432-449 ◽  
Author(s):  
E. Brink ◽  
E. Jankowska ◽  
B. Skoog
Keyword(s):  
Muscle Afferents ◽  
Primary Afferent Depolarization ◽  
Primary Afferent ◽  
Neuronal Populations ◽  
Ia Afferents ◽  
Group I ◽  
Spatial Facilitation ◽  
Low Threshold ◽  
Group I Afferents ◽  
Dorsal Root Potentials

The aim of the study was to investigate whether common or independent neuronal pathways are used to evoke primary afferent depolarization (PAD) from selectively activated group Ia and Ib afferents of different muscles. To this end, the spatial facilitation of effects of various afferents, indicating convergence on the same interneurons, was used as a test. Its occurrence was assessed on dorsal root potentials (DRPs) evoked in unspecified fibers or using intra-axonal recording from identified group Ia muscle spindle afferents or group Ib tendon organ afferents. Spatial facilitation has been found in PAD pathways a) from various Ia-afferents, whether of flexors or extensors; b) from various Ib-afferents, whether of flexors or extensors; and c) from flexor Ib-afferents and flexor or extensor Ia-afferents. In contrast, no indications have been found for common pathways from extensor Ib- and any Ia-afferents under conditions that proved effective in other combinations. Latencies of those components of PAD that appeared as a result of the spatial facilitation ranged from 2 to more than 7 ms, indicating that the convergence occurred in the shortest (trisynaptic) as well as longer pathways. The same patterns of convergence have been found in PAD pathways to extensor and flexor Ia-afferents (in experiments with intraaxonal recording from these afferents). The possibility might thus be considered that some neuronal pathways are used to modulate transmission via Ia-afferents independently of their muscle origin. The same might hold true for extensor and flexor Ib-afferents. Generally, it is concluded that the minimal number of distinct neuronal populations subserving PAD of group I afferents may be two to six. Additionally, actions of cutaneous, joint, and interosseous afferents on DRPs from Ia-afferents were reexamined to further the comparison between neurons mediating PAD and those mediating postsynaptic excitation or inhibition of motoneurons. Only depression of Ia DRPs followed stimulation of these afferents at intensities of 1.5-2.0 times threshold and higher; lower threshold afferents were apparently ineffective. On the basis of lack of convergence of extensor Ib and Ia muscle afferents and of low-threshold cutaneous afferents, interneurons mediating PAD may thus be distinguished from the interneurons subserving Ib and Ia-like-Ib postsynaptic actions in motoneurons. The latter are coexcited by these three groups of afferents.

scholarly journals Direct evidence for decreased presynaptic inhibition evoked by PBSt group I muscle afferents after chronic SCI and recovery with step-training in the decerebrated rat

2020 ◽  
Author(s):  
Guillaume Caron ◽  
Jadwiga N. Bilchak ◽  
Marie-Pascale Côté
Keyword(s):  
Presynaptic Inhibition ◽  
H Reflex ◽  
Muscle Group ◽  
Spinal Reflex ◽  
Primary Afferent Depolarization ◽  
Flexor Muscle ◽  
Primary Afferent ◽  
Reflex Excitability ◽  
Group I ◽  
Group I Afferents

ABSTRACTSpinal cord injury (SCI) results in the disruption of supraspinal control of spinal networks and an increase in the relative influence of afferent feedback to sublesional neural networks, both of which contribute to enhancing spinal reflex excitability. Hyperreflexia occurs in ~75% of individuals with chronic SCI and critically hinders functional recovery and quality of life. It is suggested to result from an increase in motoneuronal excitability and a decrease in presynaptic and postsynaptic inhibitory mechanisms. In contrast, locomotor training decreases hyperreflexia by restoring presynaptic inhibition.Primary afferent depolarization (PAD) is a powerful presynaptic inhibitory mechanism that selectively gates primary afferent transmission to spinal neurons to adjust reflex excitability and ensure smooth movement. However, the effect of chronic SCI and step-training on the reorganization of presynaptic inhibition evoked by hindlimb afferents, and the contribution of PAD has never been demonstrated. The objective of this study is to directly measure changes in presynaptic inhibition through dorsal root potentials (DRPs) and its association to plantar H-reflex inhibition. We provide direct evidence that H-reflex hyperexcitability is associated with a decrease in transmission of PAD pathways activated by PBSt afferents after chronic SCI. More precisely, we illustrate that PBSt group I muscle afferents evoke a similar pattern of inhibition onto both L4-DRPs and plantar H-reflexes evoked by the tibial nerve in Control and step-trained animals, but not in chronic SCI rats. These changes are not observed after step-training, suggesting a role for activity-dependent plasticity to regulate PAD pathways activated by flexor muscle group I afferents.Key point summaryPresynaptic inhibition is modulated by supraspinal centers and primary afferents in order to filter sensory information, adjust spinal reflex excitability, and ensure smooth movements.After SCI, the supraspinal control of primary afferent depolarization (PAD) interneurons is disengaged, suggesting an increased role for sensory afferents. While increased H-reflex excitability in spastic individuals indicates a possible decrease in presynaptic inhibition, it remains unclear whether a decrease in sensory-evoked PAD contributes to this effect.We investigated whether the PAD evoked by hindlimb afferents contributes to the change in presynaptic inhibition of the H-reflex in a decerebrated rat preparation. We found that chronic SCI decreases presynaptic inhibition of the plantar H-reflex through a reduction in PAD evoked by PBSt muscle group I afferents.We further found that step-training restored presynaptic inhibition of the plantar H-reflex evoked by PBSt, suggesting the presence of activity-dependent plasticity of PAD pathways activated by flexor muscle group I afferents.

Control of transmission in muscle group IA afferents during fictive locomotion in the cat

1996 ◽  
Vol 76 (6) ◽  
pp. 4104-4112 ◽  
Author(s):  
J. P. Gossard
Keyword(s):  
Presynaptic Inhibition ◽  
Medial Gastrocnemius ◽  
Monosynaptic Reflex ◽  
Primary Afferent Depolarization ◽  
Fictive Locomotion ◽  
Primary Afferent ◽  
Decerebrate Cat ◽  
Reflex Pathway ◽  
Ia Afferents ◽  
Sensory Evoked

1. Primary afferent depolarization (PAD) can be evoked by sensory volleys, supraspinal commands, or the activity of spinal locomotor networks (locomotor-related PAD). In this study we investigated the effect of locomotor-related PAD and of sensory-evoked PAD on the monosynaptic transmission between the group IA muscle afferents and motoneurons in the lumbosacral spinal cord. 2. Six pairs of group IA afferents and motoneurons [4 tibialis anterior (TA), 1 medial gastrocnemius (MG), 1 lateral gastrocnemius-soleus (LGS)] were successfully recorded intracellularly during spontaneous fictive locomotion in the decerebrate cat. The membrane potentials of TA axons and motoneurons were maximally depolarized during the flexor phase of the locomotor cycle. In MG and LGS pairs, the maximum depolarization in IA axons occurred during the flexor phase and, in motoneurons, during the extensor phase. There were no antidromic discharges in the recorded axons. The effects of locomotor-related PAD on IA transmission were evaluated by comparing the unitary excitatory postsynaptic potentials (EPSPs) in the motoneuron evoked by the spontaneous orthodromic firing of the group IA axon during the flexor and extensor phases, respectively. In TA pairs, the maximum amplitude of unitary EPSPs occurred during the flexor phase when the motoneuron and the axon were maximally depolarized. In the MG and LGS pairs, the maximal amplitude of unitary EPSPs occurred during the extensor phase when the motoneuron was maximally depolarized and when the axon was the least depolarized. Overall, the amplitude of unitary EPSPs was clearly modulated during the fictive step cycle and always reached a maximum during the depolarized phase of the motoneuron, whether the group IA axon was maximally depolarized or not during that phase. 3. The effect of sensory-evoked PAD on synaptic transmission was also studied in nonlocomoting preparations. One TA pair was successfully recorded and PADs were evoked by the stimulation of a peripheral nerve. The amplitude of unitary EPSPs in the motoneuron was greatly depressed during the PADs. This result is a direct demonstration of the presynaptic inhibition associated with the sensory-evoked PAD in the monosynaptic reflex pathway of the cat. 4. We conclude from these results that the locomotor-related PAD did not contribute significantly to the modulation of transmission in the monosynaptic reflex pathway of the cat during fictive locomotion. On the other hand, the results confirmed that PAD evoked by sensory input decreases group IA afferent transmission efficiently most probably by presynaptic inhibition. The results suggest therefore that, during real locomotion, sensory feedback induced by the moving limbs or perturbations will evoke an important presynaptic inhibition of the release from group IA primary afferent terminals.

Absence of effects of contralateral group I muscle afferents on presynaptic inhibition of Ia terminals in humans and cats

2012 ◽  
Vol 108 (4) ◽  
pp. 1176-1185 ◽  
Author(s):  
Rinaldo André Mezzarane ◽  
André Fabio Kohn ◽  
Erika Couto-Roldan ◽  
Lourdes Martinez ◽  
Amira Flores ◽  
...  
Keyword(s):  
Presynaptic Inhibition ◽  
Muscle Afferents ◽  
H Reflex ◽  
Triceps Surae ◽  
Reflex Response ◽  
Current View ◽  
Tendon Vibration ◽  
Vibratory Stimulus ◽  
Group I ◽  
Group I Afferents

Crossed effects from group I afferents on reflex excitability and their mechanisms of action are not yet well understood. The current view is that the influence is weak and takes place indirectly via oligosynaptic pathways. We examined possible contralateral effects from group I afferents on presynaptic inhibition of Ia terminals in humans and cats. In resting and seated human subjects the soleus (SO) H-reflex was conditioned by an electrical stimulus to the ipsilateral common peroneal nerve (CPN) to assess the level of presynaptic inhibition (PSI_control). A brief conditioning vibratory stimulus was applied to the triceps surae tendon at the contralateral side (to activate preferentially Ia muscle afferents). The amplitude of the resulting H-reflex response (PSI_conditioned) was compared to the H-reflex under PSI_control, i.e., without the vibration. The interstimulus interval between the brief vibratory stimulus and the electrical shock to the CPN was −60 to 60 ms. The H-reflex conditioned by both stimuli did not differ from that conditioned exclusively by the ipsilateral CPN stimulation. In anesthetized cats, bilateral monosynaptic reflexes (MSRs) in the left and right L7 ventral roots were recorded simultaneously. Conditioning stimulation applied to the contralateral group I posterior biceps and semitendinosus (PBSt) afferents at different time intervals (0–120 ms) did not have an effect on the ipsilateral gastrocnemius/soleus (GS) MSR. An additional experimental paradigm in the cat using contralateral tendon vibration, similar to that conducted in humans, was also performed. No significant differences between GS-MSRs conditioned by ipsilateral PBSt stimulus alone and those conditioned by both ipsilateral PBSt stimulus and contralateral tendon vibration were detected. The present results strongly suggest an absence of effects from contralateral group I fibers on the presynaptic mechanism of MSR modulation in relaxed humans and anesthetized cats.

scholarly journals Muscle afferent excitability testing in spinal root-intact rats: dissociating peripheral afferent and efferent volleys generated by intraspinal microstimulation

2017 ◽  
Vol 117 (2) ◽  
pp. 796-807 ◽  
Author(s):  
Saeka Tomatsu ◽  
Geehee Kim ◽  
Joachim Confais ◽  
Kazuhiko Seki
Keyword(s):  
Spinal Cord ◽  
Presynaptic Inhibition ◽  
Muscle Afferents ◽  
Primary Afferents ◽  
Medial Gastrocnemius ◽  
Primary Afferent Depolarization ◽  
Spinal Root ◽  
Primary Afferent ◽  
Intraspinal Microstimulation ◽  
Spinal Roots

Presynaptic inhibition of the sensory input from the periphery to the spinal cord can be evaluated directly by intra-axonal recording of primary afferent depolarization (PAD) or indirectly by intraspinal microstimulation (excitability testing). Excitability testing is superior for use in normal behaving animals, because this methodology bypasses the technically challenging intra-axonal recording. However, use of excitability testing on the muscle or joint afferent in intact animals presents its own technical challenges. Because these afferents, in many cases, are mixed with motor axons in the peripheral nervous system, it is crucial to dissociate antidromic volleys in the primary afferents from orthodromic volleys in the motor axon, both of which are evoked by intraspinal microstimulation. We have demonstrated in rats that application of a paired stimulation protocol with a short interstimulus interval (ISI) successfully dissociated the antidromic volley in the nerve innervating the medial gastrocnemius muscle. By using a 2-ms ISI, the amplitude of the volleys evoked by the second stimulation was decreased in dorsal root-sectioned rats, but the amplitude did not change or was slightly increased in ventral root-sectioned rats. Excitability testing in rats with intact spinal roots indicated that the putative antidromic volleys exhibited dominant primary afferent depolarization, which was reasonably induced from the more dorsal side of the spinal cord. We concluded that excitability testing with a paired-pulse protocol can be used for studying presynaptic inhibition of somatosensory afferents in animals with intact spinal roots. NEW & NOTEWORTHY Excitability testing of primary afferents has been used to evaluate presynaptic modulation of synaptic transmission in experiments conducted in vivo. However, to apply this method to muscle afferents of animals with intact spinal roots, it is crucial to dissociate antidromic and orthodromic volleys induced by spinal microstimulation. We propose a new method to make this dissociation possible without cutting spinal roots and demonstrate that it facilitates excitability testing of muscle afferents.

γ-Aminobutyric acid and primary afferent depolarization in feline spinal cord

1979 ◽  
Vol 57 (10) ◽  
pp. 1157-1167 ◽  
Author(s):  
B. R. Sastry
Keyword(s):  
Spinal Cord ◽  
Nerve Stimulation ◽  
Muscle Afferents ◽  
Aminobutyric Acid ◽  
Primary Afferent Depolarization ◽  
Antidromic Activation ◽  
Primary Afferent ◽  
Afferent Terminal ◽  
Group I ◽  
Terminal Excitability

The effects of iontophoretically applied γ-aminobutyric acid (GABA), (−)-nipecotic acid (NCA), 2,4-diaminobutyric acid (DABA), and pentobarbital were examined on the thresholds for antidromic activation of single group I muscle afferents, in decerebrated spinal cats. GABA decreased the threshold for antidromic activation of the majority of the afferents. During this decrease in the threshold, the preterminal axons were depolarized. This depolarization was decreased by a prior depolarization, but increased by a hyperpolarization, of the afferent. During the depolarization of the afferent produced by GABA, the size of the orthodromic action potential was decreased. Iontophoretically applied bicuculline antagonized the effect of GABA on the threshold for antidromic activation of the afferents. NCA, DABA, and pentobarbital potentiated the action of GABA on the afferent terminal excitability. Pre-treatment of the animals with semicarbazide, which reportedly depletes spinal GABA, resulted in a reduction in the threshold produced by a conditioning stimulation of other group I afferents. GABA decreased the threshold for antidromic activation of the nonterminal regions of the afferents when applied near the stimulation sites. The amounts of GABA required to produce a decrease in the threshold of the nonterminal afferents were greater than those required to produce a comparable effect on the terminal regions of the fibres. Iontophoretically applied NCA and bicuculline, in amounts that were adequate to alter the effects of applied GABA, failed to affect the nerve stimulation-induced decrease in the threshold for antidromic activation of the fibres. Intravenously injected bicuculline, however, antagonized the actions of GABA as well as of the reduction in the threshold produced by nerve stimulation.These results indicate that (1) GABA-induced increase in the excitability of group I afferent terminals is associated with a depolarization of the afferent, (2) the uptake of iontophoretically applied amino acid into the spinal cord tissue appears to limit its action on the afferent terminal excitability, (3) GABA has a preterminal depolarizing action on group I muscle afferents, and (4) primary afferent depolarization produced by nerve stimulation may be of diffuse origin and, hence, cannot be significantly affected by iontophoretically applied NCA and bicuculline.

Declining inhibition elicited in cat lumbar motoneurons by repetitive stimulation of group II muscle afferents

1993 ◽  
Vol 70 (5) ◽  
pp. 1805-1810 ◽  
Author(s):  
J. Lafleur ◽  
D. Zytnicki ◽  
G. Horcholle-Bossavit ◽  
L. Jami
Keyword(s):  
Muscle Afferents ◽  
Repetitive Stimulation ◽  
Excitatory Postsynaptic Potential ◽  
Constant Input ◽  
Rapid Reduction ◽  
Group I ◽  
Constant Strength ◽  
Group I Afferents ◽  
Group Ii ◽  
Stimulation Of

1. The aim of the present experiments was to verify whether group II inputs from gastrocnemius medialis (GM) muscle could elicit declining inhibitions similar to those observed during GM contractions in a variety of lumbar motoneurons of the cat spinal cord. Motoneurons were recorded intracellularly in chloralose- or pentobarbitone-anesthetized preparations during electrical stimulation of GM nerve with repetitive trains. 2. With strengths in the group I range, repetitive stimulation evoked the usual Ia excitation in homonymous motoneurons and excitatory postsynaptic potential (EPSP) amplitudes remained constant throughout the stimulation sequence. In synergic plantaris motoneurons lacking an excitatory connection with Ia afferents from GM, the same stimulation, kept at a constant strength throughout the stimulation sequence, elicited rapidly decreasing inhibitory potentials reminiscent of those evoked by GM contractions. 3. In motoneurons of pretibial flexors, quadriceps, and posterior biceps-semitendinosus, the stimulation strength required to observe declining inhibitions resembling those produced by GM contractions was 4-8 times group I threshold, engaging group II in addition to group I fibers. 4. These results show that input from GM group II plus group I afferents can elicit inhibitory effects in a variety of motoneurons. Such observations support the hypothesis that messages from spindle secondary endings and/or nonspecific muscle receptors activated during contraction might contribute to the widespread inhibition caused by GM contractions. 5. Inasmuch as constant input in group II and group I afferents evoked declining inhibitory potentials, the origin of the decline must be central, which suggests that the rapid reduction of contraction-induced inhibitions also depended on a central mechanism.

Synaptic organization of defined motor-unit types in cat tibialis anterior

1980 ◽  
Vol 43 (6) ◽  
pp. 1631-1644 ◽  
Author(s):  
R. P. Dum ◽  
T. T. Kennedy
Keyword(s):  
Motor Unit ◽  
Tibialis Anterior ◽  
Muscle Afferents ◽  
Medial Gastrocnemius ◽  
Synaptic Organization ◽  
Ia Afferents ◽  
Group I ◽  
Ia Epsp ◽  
Group I Afferents ◽  
Stimulation Of

1. Synaptic potentials were recorded intracellularly in tibialis anterior (TA) motoneurons following stimulation of a descending brain stem pathway, the medial longitudinal fasciculus (MLF), and three segmental inputs, the homonymous and heteronymous group Ia afferents, the group I afferents from the antagonist, and the cutaneous and muscle afferents. Intracellular stimulation of the motoneurons was used to classify them, based on the properties of the innervated muscle units, into types FF, F(int), FR, and S (6, 16). 2. The sum of the monosynaptic EPSP amplitudes resulting from stimulation of homonymous and heteronymous group Ia afferents (summed group Ia EPSP) was inversely related to motoneuron size, as assessed by motoneuron input resistance, and was inversely related to motor-unit tetanic tension. Type-FF, -FR, and -S motoneurons showed significant differences in the mean amplitude of their summed group Ia EPSPs. 3. The amplitudes of disynaptic IPSPs resulting from stimulation of group I afferents in the antagonist muscle also showed an inverse relationship to motoneuron size. The observed relationships between motoneuron size and the monosynaptic group Ia EPSP amplitude or the disynaptic group I IPSP amplitude are compatible with the “size principle” of motor-unit recruitment (26). 4. The amplitudes of the monosynaptic EPSPs evoked in TA motoneurons by stimulation of the MLF were distributed rather randomly among all types of TA motoneurons. A slight tendency of larger monosynaptic EPSPs to occur in motoneurons with larger tetanic tensions was observed. 5. The polysynaptic effects from cutaneous and muscle afferents in sural and gastrocnemius-soleus nerves were frequently excitatory on type-FF motoneurons, but were primarily inhibitory on type-FR and -S motoneurons. Clearly, the polysynaptic cutaneous and muscle inputs and the monosynaptic MLF input onto TA motoneurons show a different pattern of synaptic organization than the group I inputs. 6. In general, the synaptic organization of the TA motor nucleus is similar to that of its extensor antagonist, medial gastrocnemius (MG) (2--5, 7, 8), when analogous neural circuits are compared. This parallel organization suggests a commonality of motor-control systems for both flexor and extensor muscles.

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