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.

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.

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.

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.

Changes in H-reflex amplitude to muscle stretch and lengthening in humans

2016 ◽  
Vol 27 (5) ◽  
pp. 511-522 ◽  
Author(s):  
Francesco Budini ◽  
Markus Tilp
Keyword(s):  
Human Movement ◽  
Careful Consideration ◽  
H Reflex ◽  
Spinal Reflex ◽  
Neural Pathways ◽  
Static Stretching ◽  
Plantar Flexors ◽  
Reflex Excitability ◽  
Apparent Disagreement ◽  
Shed Light

AbstractSpinal reflex excitability is traditionally assessed to investigate neural adjustments that occur during human movement. Different experimental procedures are known to condition spinal reflex excitability. Among these, lengthening movements and static stretching the human triceps have been investigated over the last 50 years. The purpose of this review is to shed light on several apparent incongruities in terms of magnitude and duration of the reported results. In the present review dissimilarities in neuro-spinal changes are examined in relation to the methodologies applied to condition and measure them. Literature that investigated three different conditioning procedures was reviewed: passive dorsiflexion, active dorsiflexion through antagonists shortening and eccentric plantar-flexors contractions. Measurements were obtained before, during and after lengthening or stretching. Stimulation intensities and time delays between conditioning procedures and stimuli varied considerably. H-reflex decreases immediately as static stretching is applied and in proportion to the stretch degree. During dorsiflexions the inhibition is stronger with greater dorsiflexion angular velocity and at lower nerve stimulation intensities, while it is weaker if any concomitant muscle contraction is performed. Within 2 s after a single passive dorsiflexion movement, H-reflex is strongly inhibited, and this effect disappears within 15 s. Dorsiflexions repeated over 1 h and prolonged static stretching training induce long-lasting inhibition. This review highlights that the apparent disagreement between studies is ascribable to small methodological differences. Lengthening movements and stretching can strongly influence spinal neural pathways. Results interpretation, however, needs careful consideration of the methodology applied.

Presynaptic inhibition in the crayfish CNS: pathways and synaptic mechanisms

1985 ◽  
Vol 54 (5) ◽  
pp. 1305-1325 ◽  
Author(s):  
M. D. Kirk
Keyword(s):  
Presynaptic Inhibition ◽  
Escape Behavior ◽  
Lucifer Yellow ◽  
Afferent Input ◽  
Abdominal Ganglion ◽  
Primary Afferent Depolarization ◽  
Direct Stimulation ◽  
Primary Input ◽  
Primary Afferent ◽  
Afferent Terminals

I studied the pathways that produce primary afferent depolarization (PAD) and presynaptic inhibition during crayfish escape behavior. Simultaneous intracellular recordings were obtained from interneurons and primary afferent axons in the neuropil of the sixth abdominal ganglion. In several experiments, a sucrose-gap recording of PAD accompanied the intracellular impalements. I have identified PAD-producing inhibitory interneurons (PADIs) that are fired by a single impulse in the lateral (LG) or medial (MG) giant, escape-command axons; the PADIs appear to be directly responsible for presynaptic inhibition of primary afferent input to identified mechanosensory interneurons. PADI spikes, elicited by injection of depolarizing current, produced unitary PAD with constant short latency (mean = 0.97 +/- 0.12 SD ms). The unitary PADs were capable of following PADI impulses one for one at frequencies greater than 100 Hz, and the amplitude of unitary PAD was increased by injection of chloride into the afferent terminals. Therefore, the PADIs appear to directly produce an increase in chloride conductance in the primary afferent terminals. Intracellular injections of Lucifer yellow or horseradish peroxidase (HRP) revealed three morphological types of PADI. Their axonal branches and terminals are bilateral and overlap extensively with the innervation fields of all 10 sensory roots of the sixth ganglion. The three morphological types of PADI were physiologically indistinguishable. In several cases, the impaled PADI was shown to produce unitary PAD in more than one afferent of a given root as well as in afferents of adjacent roots. Therefore, the PADIs appear to diverge widely and contact many afferents in all of the sixth-ganglion sensory roots. Stimulation, caudal to the fifth ganglion, of an MG that had been interrupted rostral to the fifth ganglion produced no PAD in sixth-ganglion afferents. Also, stimulation of an MG or an LG in a surgically isolated sixth abdominal ganglion failed to produce PAD. Therefore, the pathway between the MGs and PADIs is activated exclusively within the rostral abdominal ganglia. Direct stimulation in the second and third abdominal ganglia of the segmental giants (SGs) produced a polysynaptic, suprathreshold response in the PADIs. This response was compound and was not due to the activity of the identified corollary discharge interneurons, CDI-2 and CDI-3, that are fired by the SGs. Therefore, the primary input to the PADIs must come from other, unidentified CDIs that are driven by the SGs. PADIs were not fired by shocks to the sensory portions of any peripheral roots even though these shocks produced PAD.(ABSTRACT TRUNCATED AT 400 WORDS)

The Role of Primary afferent Depolarisation in Presynaptic Inhibition of Group I Fibres

1995 ◽  
pp. 334-336
Author(s):  
B. Lamotte d’Incamps ◽  
M.-L. Monnet ◽  
C. Meunier ◽  
D. Zytnicki
Keyword(s):  
Presynaptic Inhibition ◽  
Primary Afferent ◽  
Group I

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.

Primary afferent depolarization of muscle afferents elicited by stimulation of joint afferents in cats with intact neuraxis and during reversible spinalization

1993 ◽  
Vol 70 (5) ◽  
pp. 1899-1910 ◽  
Author(s):  
J. Quevedo ◽  
J. R. Eguibar ◽  
I. Jimenez ◽  
R. F. Schmidt ◽  
P. Rudomin
Keyword(s):  
Spinal Cord ◽  
Knee Joint ◽  
High Threshold ◽  
Primary Afferent Depolarization ◽  
Delayed Response ◽  
Primary Afferent ◽  
Myelinated Fibers ◽  
Group I ◽  
Posterior Knee ◽  
Stimulation Of

1. In the anesthetized and artificially ventilated cat, stimulation of the posterior articular nerve (PAN) with low strengths (1.2-1.4 x T) produced a small negative response (N1) in the cord dorsum of the lumbosacral spinal cord with a mean onset latency of 5.2 ms. Stronger stimuli (> 1.4 x T) produced two additional components (N2 and N3) with longer latencies (mean latencies 7.5 and 15.7 ms, respectively), usually followed by a slow positivity lasting 100-150 ms. With stimulus strengths above 10 x T there was in some experiments a delayed response (N4; mean latency 32 ms). 2. Activation of posterior knee joint nerve with single pulses and intensities producing N1 responses only, usually produced no dorsal root potentials (DRPs), or these were rather small. Stimulation with strengths producing N2 and N3 responses produced distinct DRPs. Trains of pulses were clearly more effective than single pulses in producing DRPs, even in the low-intensity range. 3. Cooling the thoracic spinal cord to block impulse conduction, increased the DRPs and the N3 responses produced by PAN stimulation without significantly affecting the N2 responses. Reversible spinalization also increased the DRPs produced by stimulation of cutaneous nerves. In contrast, the DRPs produced by stimulation of group I afferents from flexors were reduced. 4. Conditioning electrical stimulation of intermediate and high-threshold myelinated fibers in the PAN depressed the DRPs produced by stimulation of group I muscle and of cutaneous nerves. 5. Analysis of the intraspinal threshold changes of single Ia and Ib fibers has provided evidence that stimulation of intermediate and high threshold myelinated fibers in the posterior knee joint nerve inhibits the primary afferent depolarization (PAD) of Ia fibers, and may either produce PAD or inhibit the PAD in Ib fibers, in the same manner as stimulation of cutaneous nerves. In 7/16 group I fibers the inhibition of the PAD was increased during reversible spinalization. 6. The results obtained suggest that intermediate and high-threshold myelinated fibers in the PAN have the same actions on Ia and Ib fibers as intermediate and high-threshold cutaneous afferents and may therefore be considered as belonging to the same functional system. They further indicate that in anesthetized preparations the pathways mediating the PAD of group I fibers, as well as the pathways mediating the inhibition of the PAD, may be subjected to a descending control that is removed by spinalization.

Differential effects of a flexor nerve input on the human soleus H-reflex during standing versus walking

1995 ◽  
Vol 73 (4) ◽  
pp. 436-449 ◽  
Author(s):  
C. Capaday ◽  
B. A. Lavoie ◽  
F. Comeau
Keyword(s):  
Spinal Cord ◽  
Presynaptic Inhibition ◽  
Stance Phase ◽  
Conditioning Stimulus ◽  
Background Level ◽  
H Reflex ◽  
Emg Activity ◽  
Group I ◽  
The Difference

A conditioning (C) stimulus at group I strength was delivered during standing to the common peroneal (CP) nerve before a test (T) stimulus at several C–T intervals ranging from 0 to 150 ms. At sufficiently long C–T intervals (100–120 ms) the soleus H-reflex was strongly inhibited despite little, or no change, in the background level of EMG activity. This finding indicates that a significant portion of the inhibition occurs at a premotoneuronal level, likely via presynaptic inhibition of the Ia-afferent terminals. During standing, at C–T intervals of 100–120 ms (optimal C–T interval) a conditioning stimulus to the CP nerve of 1.5 times motor threshold (MT) intensity reduced the soleus H-reflex by an average of 45.8% (n = 14 subjects). The conditioning stimulus always produced a clear inhibition of the H-reflex during standing at these C–T intervals. The effects of this conditioning stimulus on the soleus H-reflex were then determined in the early part of the stance phase of walking. In contrast to standing, the conditioning stimulus produced little or no inhibition during the early part of the stance phase of walking (average inhibition 45.8 vs. 11.6%, n = 14 subjects). The soleus background EMG, and the soleus and tibialis anterior M-waves were essentially the same during standing and walking. Furthermore, there was no shift of the optimal C–T interval during walking. The difference in the effects of the conditioning stimulus was not due to differences in the size of the test H-reflex in each task. It appears to be due to a genuine task-dependent change in the input–output properties of the underlying spinal cord circuits. There are at least two, mutually compatible, explanations of these results. Firstly, during walking the intraspinal terminals of the afferent fibres (group Ia and Ib) conducting the conditioning volley may be presynaptically inhibited, or their input gated at the interneuronal level. Secondly, on the assumption that the conditioning stimulus is acting via the presynaptic inhibitory network in the spinal cord, it is possible that during walking this network is saturated as a result of increased central or peripheral synaptic inputs. Finally, it seems unlikely that differences in the refractoriness of the CP nerve between the tasks may be involved; the reasons for this are presented in the discussion.Key words: Ia afferents, motoneurons, presynaptic inhibition, EMG, posture, locomotion, spinal cord.

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