Small-caliber afferent inputs produce a heterosynaptic facilitation of the synaptic responses evoked by primary afferent A-fibers in the neonatal rat spinal cord in vitro

1993 ◽  
Vol 69 (6) ◽  
pp. 2116-2128 ◽  
Author(s):  
S. W. Thompson ◽  
C. J. Woolf ◽  
L. G. Sivilotti
Keyword(s):  
Spinal Cord ◽  
Dorsal Root ◽  
Fiber Strength ◽  
Conditioning Stimulus ◽  
Neonatal Rat ◽  
Primary Afferent ◽  
Synaptic Potentials ◽  
C Fiber ◽  
Afferent Inputs

1. The effect of brief primary afferent inputs on the amplitude and duration of the synaptic potentials evoked in ventral horn (VH) neurons by the activation of other unconditioned primary afferents was studied by current-clamp intracellular recording in the neonatal rat hemisected spinal cord in vitro. Low-frequency (1 Hz) trains of stimulation were applied to a lumbar dorsal root (Conditioning root) for 20-30 s. Test excitatory synaptic potentials (EPSPs) were evoked by single electrical shocks applied to an adjacent Test dorsal root. 2. Test and Conditioning inputs were generated at stimulation strengths sufficient to activate A beta-, A delta- and C-afferent fibers successively. At A delta- and C-fiber strength the EPSPs lasted for 4-6 s, and, during the repetitive Conditioning inputs, these summated to produce a progressively incrementing cumulative depolarization that slowly decayed back to the control Vm over tens of seconds. 3. Dorsal root conditioning produced heterosynaptic facilitation, defined as an enhancement of Test EPSPs above their DC matched controls, in 7 out of 20 neurons. To facilitate the unconditioned afferent input, the intensity of conditioning stimulation had to exceed the threshold for the activation of thin myelinated (A delta) afferents: conditioning at A beta-fiber strength had no effect, whereas A delta- and C-fiber strength conditioning were equally effective. 4. Heterosynaptic facilitation of only A beta- or A delta-fiber-evoked Test EPSPs was observed, no enhancement of C-fiber strength Test EPSPs could be demonstrated. The facilitation manifested as increases in the EPSP peak amplitude, area or the number of action potentials evoked. 5. Conditioning trials that produced heterosynaptic facilitation generated cumulative depolarizations larger than those produced by ineffective conditioning trials (9.1 +/- 3.1 vs. 3.3 +/- 0.5 mV after 20 s conditioning at resting Vm, mean +/- SE, n = 6 and 13, respectively; P < 0.05). The slope of the Vm trajectory during the summation of the conditioning EPSPs was higher in trials resulting in heterosynaptic facilitation, at 0.31 +/- 0.10 mV/s in neurons with heterosynaptic facilitation and 0.06 +/- 0.02 mV/s in cells without heterosynaptic facilitation (P < 0.05). 5. Four of the 20 VH neurons in our sample responded to A delta/C-fiber conditioning with action-potential windup: all 4 also displayed heterosynaptic facilitation. 6. Heterosynaptic facilitation decayed after the completion of the conditioning stimulus with a time course that was parallel to but not superimposable on that of the slow Vm depolarization evoked by the conditioning.(ABSTRACT TRUNCATED AT 400 WORDS)

Modulation of monosynaptic excitation in the neonatal rat spinal cord

1993 ◽  
Vol 70 (3) ◽  
pp. 1151-1158 ◽  
Author(s):  
M. Pinco ◽  
A. Lev-Tov
Keyword(s):  
Spinal Cord ◽  
Dorsal Root ◽  
Neonatal Rat ◽  
Bathing Solution ◽  
Duration Stimulus ◽  
Low Calcium ◽  
Dorsal Root Afferents ◽  
Stimulation Of ◽  
Monosynaptic Excitation

1. The effects of high-frequency (5-50 Hz) stimulation of dorsal root afferents on monosynaptic excitation of alpha motoneurons was studied in the in vitro spinal cord preparation of the neonatal rat, using sharp-electrode intracellular recordings. 2. Double pulse stimulation of dorsal root afferents induced severe depression of testing excitatory postsynaptic potentials (EPSPs) at each of the tested interstimulus intervals (15 ms-5 s). After perfusion of the preparation with low-calcium, high-magnesium Krebs saline, the amplitude of the conditioning EPSPs was markedly decreased and the testing EPSPs exhibited substantial facilitation that was maximal at the 20-ms interval and that was accompanied by depression at intervals > or = 60-100 ms. 3. Short-duration stimulus trains applied to dorsal root afferents normally induced tetanic depression of the intracellularly recorded monosynaptic EPSPs. Switching the bathing solution to low-calcium, high-magnesium saline decreased the control EPSP and induced facilitation and then tetanic potentiation (TP) of the EPSPs within the applied train. The magnitude of potentiation (% potentiation) of these EPSPs depended on the interpulse interval of the short stimulus train and on the degree of attenuation of the unpotentiated control EPSP after the solution was changed from normal- to low-calcium Krebs solution. 4. Long-duration stimulus trains applied to dorsal root afferents at 5-10 Hz induced marked depression of monosynaptic EPSPs during the train. The depression was alleviated after cessation of the tetanic stimulation and was followed in some cases by slight posttetanic potentiation.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Afferent Inputs Modulate the Activity of a Rhythmic Burst Generator in the Rat Disinhibited Spinal Cord In Vitro

1997 ◽  
Vol 77 (6) ◽  
pp. 3157-3167 ◽  
Author(s):  
E. Bracci ◽  
M. Beato ◽  
A. Nistri
Keyword(s):  
Spinal Cord ◽  
Burst Duration ◽  
Neonatal Rat ◽  
Rhythmic Pattern ◽  
Synaptic Inputs ◽  
Electrical Pulses ◽  
Afferent Inputs ◽  
Spontaneous Bursts ◽  
Rhythmic Burst

Bracci, E., M. Beato, and A. Nistri. Afferent inputs modulate the activity of a rhythmic burst generator in the rat disinhibited spinal cord in vitro. J. Neurophysiol. 77: 3157–3167, 1997. Application of strychnine and bicuculline to the isolated spinal cord of the neonatal rat induces spontaneous bursting of regular rhythmicity (cycle period ∼30 s). This phenomenon is important because it shows that a spinal network, made up by excitatory connections only, generates a very reliable rhythmic pattern. To find out how signals from the periphery or higher centres might influence the operation of the rhythmogenic network, the present experiments examined whether synaptic inputs from dorsal root (DR) or ventrolateral (VL) afferent fibers could modulate this spontaneous rhythmicity. This issue was addressed with intracellular recording from motoneurons or extracellular recording from ventral roots after eliciting bursting with strychnine plus bicuculline. Single electrical shocks (0.1 ms; intensity 1–4 times threshold) applied to one DR reset spontaneous bursting without altering its period or duration. Repetitive stimulations at periods ranging from 20 to 2 s entrained bursts on a 1:1 basis. Burst duration was shorter at lower stimulation periods whereas burst amplitude was unchanged. The lowest stimulation period compatible with burst entrainment depended on stimulus strength. At stimulation periods <2-s entrainment was always lost and spontaneous bursts unexpectedly returned even if electrical pulses still elicited ventral root reflexes. Such spontaneous bursts had similar properties as those recorded in the absence of electrical pulses. Analogous results were obtained with VL stimulations. It is concluded that the spinal rhythmogenic network was highly susceptible to external synaptic inputs, which paced burst generation whereas burst duration was adapted to interstimulus interval. A scheme is provided to explain the modulatory role of synaptic inputs as well as the escape of bursting from fast stimulus entrainment in terms of a rhythmogenic network functionally separated from reflex pathways activated by DR or VL tracts.

α5GABAA receptors mediate primary afferent fiber tonic excitability in the turtle spinal cord

2013 ◽  
Vol 110 (9) ◽  
pp. 2175-2184 ◽  
Author(s):  
Emanuel Loeza-Alcocer ◽  
Martha Canto-Bustos ◽  
Justo Aguilar ◽  
Ricardo González-Ramírez ◽  
Ricardo Felix ◽  
...  
Keyword(s):  
Spinal Cord ◽  
Dorsal Root Ganglia ◽  
Dorsal Root ◽  
Afferent Fiber ◽  
Primary Afferents ◽  
Equilibrium Potential ◽  
Primary Afferent Depolarization ◽  
Primary Afferent ◽  
Dorsal Root Reflex

γ-Amino butyric acid (GABA) plays a key role in the regulation of central nervous system by activating synaptic and extrasynaptic GABAA receptors. It is acknowledged that extrasynaptic GABAA receptors located in the soma, dendrites, and axons may be activated tonically by low extracellular GABA concentrations. The activation of these receptors produces a persistent conductance that can hyperpolarize or depolarize nerve cells depending on the Cl− equilibrium potential. In an in vitro preparation of the turtle spinal cord we show that extrasynaptic α5GABAA receptors mediate the tonic state of excitability of primary afferents independently of the phasic primary afferent depolarization mediated by synaptic GABAA receptors. Blockade of α5GABAA receptors with the inverse agonist L-655,708 depressed the dorsal root reflex (DRR) without affecting the phasic increase in excitability of primary afferents. Using RT-PCR and Western blotting, we corroborated the presence of the mRNA and the α5GABAA protein in the dorsal root ganglia of the turtle spinal cord. The receptors were localized in primary afferents in dorsal root, dorsal root ganglia, and peripheral nerve terminals using immunoconfocal microscopy. Considering the implications of the DRR in neurogenic inflammation, α5GABAA receptors may serve as potential pharmacological targets for the treatment of pain.

scholarly journals Glucose is an adequate energy substrate for the depolarizing action of GABA and glycine in the neonatal rat spinal cord in vitro

2012 ◽  
Vol 107 (11) ◽  
pp. 3107-3115 ◽  
Author(s):  
Rémi Bos ◽  
Laurent Vinay
Keyword(s):  
Spinal Cord ◽  
Energy Supply ◽  
Reversal Potential ◽  
Neonatal Rat ◽  
Lumbar Spinal Cord ◽  
Primary Afferent ◽  
Artificial Cerebrospinal Fluid ◽  
High Concentrations ◽  
Lumbar Spinal

In vitro studies have repeatedly demonstrated that the neurotransmitters γ-aminobutyric acid (GABA) and glycine depolarize immature neurons in many areas of the CNS, including the spinal cord. This widely accepted phenomenon was recently challenged by experiments showing that the depolarizing action of GABA on neonatal hippocampus and neocortex in vitro was prevented by adding energy substrates (ES), such as the ketone body metabolite dl-β-hydroxybutyric acid (DL-BHB), lactate, or pyruvate to the artificial cerebrospinal fluid (ACSF). It was suggested that GABA-induced depolarizations in vitro might be an artifact due to inadequate energy supply when glucose is the sole energy source, consistent with the energy metabolism of neonatal rat brain being largely dependent on ESs other than glucose. Here we examined the effects of these ESs (DL-BHB, lactate, pyruvate) on inhibitory postsynaptic potentials (IPSPs) recorded from neonatal rat lumbar spinal cord motoneurons (MNs), in vitro. We report that supplementing the ACSF with physiologic concentrations of DL-BHB, lactate, or pyruvate does not alter the reversal potential of IPSPs ( EIPSP). Only high concentrations of pyruvate hyperpolarized EIPSP. In addition, the depolarizing action of GABA on primary afferent terminals was not affected by supplementing the ACSF with ES at physiologic concentrations. We conclude that depolarizing IPSPs in immature MNs and the primary afferent depolarizations are not caused by inadequate energy supply. Glucose at its standard concentration appears to be an adequate ES for the neonatal spinal cord in vitro.

Neural mechanisms generating respiratory pattern in mammalian brain stem-spinal cord in vitro. I. Spatiotemporal patterns of motor and medullary neuron activity

1990 ◽  
Vol 64 (4) ◽  
pp. 1149-1169 ◽  
Author(s):  
J. C. Smith ◽  
J. J. Greer ◽  
G. S. Liu ◽  
J. L. Feldman
Keyword(s):  
Spinal Cord ◽  
Brain Stem ◽  
High Frequency ◽  
Neonatal Rat ◽  
Amplitude Fluctuations ◽  
Frequency Components ◽  
Afferent Inputs ◽  
Synaptic Drive

1. An analysis of the spatial and temporal patterns of activity of neurons of the respiratory motor-pattern generation system in an in vitro neonatal rat brain stem-spinal cord preparation is presented. Impulse discharge patterns of spinal and cranial moto-neurons as well as respiratory neurons in the medulla were analyzed. Patterns of motoneuronal discharge were characterized at the population level from recordings of motor-nerve discharge and at the single-cell level from intracellular recordings. These patterns were compared to patterns generated in the neonatal rat and adult mammal in vivo to establish the correspondence between in vitro and in vivo states. 2. The in vitro system generated a complex spatiotemporal pattern of spinal and cranial motoneuron activity during inspiratory (I) and expiratory (E) phases of the respiratory cycle. The respiratory cycle consisted of three distinct phases of neuronal activity (I, early E, and late E phase) similar to the temporal organization of the cycle in the intact mammal. The spike discharge pattern of motoneurons during the I phase consisted of a rapidly peaking-slowly decrementing discharge envelope with a high degree of synchronization on a time scale of 25-50 ms (approximately 20-40 Hz). A similar pattern was generated in the neonate in vivo under conditions comparable with the in vitro state (i.e., nervous system isolated from mechanosensory afferent inputs). However, the I-phase-motoneuron discharge pattern and cycle-phase durations differed from those characteristic of the intact neonatal or adult systems in vivo. This difference could be accounted for primarily by removal of vagal mechanosensory afferent inputs. 3. The synaptic drive potentials of spinal motoneurons during the I phase in vitro consisted of a rapidly peaking-slowly decrementing potential envelope similar in shape to the spike-frequency histogram of single motoneurons and the envelope of the motoneuron-population discharge. The drive potentials had prominent high-frequency amplitude fluctuations superimposed on the slower drive-potential envelope that were temporally correlated with the generation of motoneuron action potentials. The dominant frequency components of these fast-membrane-potential oscillations (20-35 Hz) were similar to the frequency components of the amplitude fluctuations in the motoneuron-population discharge. One class of medullary neurons with I-phase discharge also exhibited a rapidly peaking-slowly decrementing pattern of impulse discharge and synaptic drive potential with similar high-frequency components.(ABSTRACT TRUNCATED AT 400 WORDS)

Neuronal Bursting Induced by NK3 Receptor Activation in the Neonatal Rat Spinal Cord In Vitro

2001 ◽  
Vol 86 (6) ◽  
pp. 2939-2950 ◽  
Author(s):  
Cristina Marchetti ◽  
Andrea Nistri
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Dorsal Root ◽  
Extracellular Recording ◽  
Rhythmic Activity ◽  
Input Resistance ◽  
Receptor Activation ◽  
Neonatal Rat ◽  
Rat Spinal Cord

Intracellular recording from lumbar motoneurons and extracellular recording from ventral roots of the neonatal rat isolated spinal cord were used to study the mechanisms responsible for the excitation mediated by NK3 tachykinin receptors. The selective NK3 agonists senktide or [MePhe7]neurokinin B induced a slow depolarization with superimposed oscillations (mean period ± SD was 2.8 ± 0.8 s) that, in the majority of cases, showed left-right alternation at segmental level and were synchronous between L2 and L5 of the same side. During agonist wash out (5–20 min) a delayed form of hyperexcitability emerged consisting of bursts lasting 8 ± 2 s (average interburst interval 55 ± 21 s) with superimposed oscillations usually with homosegmental alternation and heterosegmental synchronicity. Such bursting was accompanied by depression of GABAergic dorsal root potentials evoked by dorsal root stimulation and of the recurrent inhibitory postsynaptic potential recorded from motoneurons. Despite bursting, motoneuron membrane potential returned to baseline while input resistance was increased. Bursts were a network-dependent phenomenon triggered by previous NK3 receptor activation because bursting was suppressed by glutamate receptor antagonists and was insensitive to motoneuron membrane potential or subsequent application of an NK3 receptor antagonist. NK3 receptors operated synergistically with N-methyl-d-aspartate (NMDA) and 5-hydroxytryptamine (5-HT) to trigger fully alternating locomotor-like rhythms while NK3 receptor antagonism disrupted the same rhythm. In summary, in the neonatal rat spinal cord NK3 receptors could trigger rhythmic activity predominantly with alternation at segmental level but with synchronous coupling between ipsilateral motor pools. NK3receptor activation could also facilitate fictive locomotor patterns induced by NMDA and 5-HT.

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