DIFFERENTIAL EXCITATION OF DORSAL HORN AND SUBSTANTIA GELATINOSA MARGINAL NEURONS BY PRIMARY AFFERENT UNITS WITH FINE (Aδ AND C) FIBERS

1976 ◽  
pp. 67-89 ◽  
Author(s):  
T. KUMAZAWA ◽  
E.R. PERL
Keyword(s):  
Dorsal Horn ◽  
Substantia Gelatinosa ◽  
Primary Afferent ◽  
C Fibers ◽  
Differential Excitation

Differential L-glutamate responsiveness among superficial dorsal horn neurons

1994 ◽  
Vol 72 (6) ◽  
pp. 2956-2965 ◽  
Author(s):  
J. Nastrom ◽  
S. P. Schneider ◽  
E. R. Perl
Keyword(s):  
Nmda Receptors ◽  
Dorsal Horn ◽  
Glutamate Uptake ◽  
Nmda Antagonist ◽  
Resting Potential ◽  
Superficial Dorsal Horn ◽  
Primary Afferent ◽  
Postsynaptic Potentials ◽  
C Fibers ◽  
The Mean

1. Intracellular recordings were made from 128 superficial dorsal horn (laminae I and II) neurons in slice preparations of the lumbosacral spinal cord obtained from young hamsters. Stimulation of the segmental dorsal root evoked postsynaptic potentials in all neurons. The average transmembrane resting potential was -61 +/- 1 mV (mean +/- SE; n = 123). The mean action potential amplitude was 75 +/- 1 mV (n = 105) with a duration at half peak of 1.1 +/- 0.1 ms (n = 102). The mean input resistance of these neurons was 72 +/- 4 M omega (n = 125). These values are comparable to those reported in other studies on neurons of this region using penetrating microelectrodes. 2. Bath application of N-methyl-D-aspartate (NMDA; 50 microM) depolarized 67 of 71 (94%) of the tested neurons. Superfusion with the non-NMDA amino acid agonists DL-alpha-amino-3-hydroxy-5-methyl-4- isoxazole propionic acid (AMPA; 20 microM) and kainate (KA; 50 microM) depolarized all tested neurons by > 10 mV. On the other hand, only 13 of 67 (19%) tested neurons were depolarized > 4 mV by superfusion solutions containing 3 mM L-glutamate (Glu). L-Aspartate at 3 mM depolarized three out of seven neurons by > 4 mV and appeared to be equally as effective as Glu. 3. The non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 10 microM) substantially attenuated the AMPA- and KA-induced depolarizations and partially attenuated the NMDA-induced depolarizations. The NMDA antagonist 3 [(+/-)-2-carboxypiperazin-4-yl]-propyl-1-phosphonic acid (CPP; 50 microM) reversibly blocked the NMDA-induced depolarization in all tested neurons. Glu-induced depolarization was unaffected by CNQX but was attenuated by CPP in three of three tested neurons. These observations indicate that some of the Glu-induced depolarization was mediated by NMDA receptors. 4. CNQX reversibly attenuated excitatory postsynaptic potentials (EPSPs) produced by primary afferent activity in A delta- and C-fibers whereas CPP suppressed only the late EPSP components. Therefore in the neurons sampled, synaptic responses evoked from primary afferent fibers appear to be mediated by both non-NMDA and NMDA receptors. 5. The glutamate uptake inhibitors, L-trans-pyrrolidine-2,4-dicarboxylate (L-trans PDC; 50 microM; n = 6) and threo-3-hydroxy-D-aspartate (1 mM; n = 1) did not have a consistent effect upon Glu action background discharge, RN or Vm in Glu-unresponsive neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Electrophysiological and Morphological Features of Rebound Depolarization Characterized Interneurons in Rat Superficial Spinal Dorsal Horn

2021 ◽  
Vol 15 ◽  
Author(s):  
Mengye Zhu ◽  
Yi Yan ◽  
Xuezhong Cao ◽  
Fei Zeng ◽  
Gang Xu ◽  
...  
Keyword(s):  
Dorsal Horn ◽  
Spinal Dorsal Horn ◽  
Morphological Characteristics ◽  
Substantia Gelatinosa ◽  
Morphological Properties ◽  
Specific Cell ◽  
Membrane Hyperpolarization ◽  
Spinal Dorsal ◽  
C Fibers ◽  
Somatosensory Information

Substantia gelatinosa (SG) neurons, which are located in the spinal dorsal horn (lamina II), have been identified as the “central gate” for the transmission and modulation of nociceptive information. Rebound depolarization (RD), a biophysical property mediated by membrane hyperpolarization that is frequently recorded in the central nervous system, contributes to shaping neuronal intrinsic excitability and, in turn, contributes to neuronal output and network function. However, the electrophysiological and morphological properties of SG neurons exhibiting RD remain unclarified. In this study, whole-cell patch-clamp recordings were performed on SG neurons from parasagittal spinal cord slices. RD was detected in 44.44% (84 out of 189) of the SG neurons recorded. We found that RD-expressing neurons had more depolarized resting membrane potentials, more hyperpolarized action potential (AP) thresholds, higher AP amplitudes, shorter AP durations, and higher spike frequencies in response to depolarizing current injection than neurons without RD. Based on their firing patterns and morphological characteristics, we propose that most of the SG neurons with RD mainly displayed tonic firing (69.05%) and corresponded to islet cell morphology (58.82%). Meanwhile, subthreshold currents, including the hyperpolarization-activated cation current (Ih) and T-type calcium current (IT), were identified in SG neurons with RD. Blockage of Ih delayed the onset of the first spike in RD, while abolishment of IT significantly blunted the amplitude of RD. Regarding synaptic inputs, SG neurons with RD showed lower frequencies in both spontaneous and miniature excitatory synaptic currents. Furthermore, RD-expressing neurons received either Aδ- or C-afferent-mediated monosynaptic and polysynaptic inputs. However, RD-lacking neurons received afferents from monosynaptic and polysynaptic Aδ fibers and predominantly polysynaptic C-fibers. These findings demonstrate that SG neurons with RD have a specific cell-type distribution, and may differentially process somatosensory information compared to those without RD.

scholarly journals Differential Presynaptic Effects of Opioid Agonists on Aδ- and C-afferent Glutamatergic Transmission to the Spinal Dorsal Horn

2007 ◽  
Vol 107 (5) ◽  
pp. 807-812 ◽  
Author(s):  
Miho Ikoma ◽  
Tatsuro Kohno ◽  
Hiroshi Baba
Keyword(s):  
Spinal Cord ◽  
Intrathecal Administration ◽  
Kappa Opioid Receptor ◽  
Substantia Gelatinosa ◽  
Patch Clamp Technique ◽  
Primary Afferent ◽  
Kappa Agonist ◽  
C Fibers ◽  
Opioid Agonists ◽  
C Fiber

Background Although intrathecal administration of opioids produces antinociceptive effects in the spinal cord, it has not been established whether intrathecal opioid application more effectively terminates C fiber-mediated pain than A fiber-mediated pain. Here, the authors focus on the differences in opioid actions on Adelta- and C-afferent responses. Methods Using the whole cell patch clamp technique, the authors investigated the presynaptic inhibitory actions of micro-, delta-, and kappa-opioid receptor agonists on primary afferent-evoked excitatory postsynaptic currents (EPSCs) in substantia gelatinosa neurons of adult rat spinal cord slices. Results The micro agonist DAMGO (0.1, 1 microM) reduced the amplitude of glutamatergic monosynaptic Adelta- or C fiber-evoked EPSCs. C fiber-evoked EPSCs were inhibited to a greater extent than Adelta fiber-evoked EPSCs. The delta agonist DPDPE (1, 10 microM) produced modest inhibition of Adelta- or C fiber-evoked EPSCs. In contrast, the kappa agonist U69593 (1 microM) did not affect the amplitude of either Adelta or C fiber-evoked EPSCs. Conclusions These results indicate that opioids suppress excitatory synaptic transmission mainly through activation of micro receptors on primary afferent C fibers. Given that the substantia gelatinosa is the main termination of Adelta and C fibers transmitting nociceptive information, the current findings may partially explain the different potency of opioid agonists.

Physiological studies of cutaneous inputs to dorsal horn laminae I-IV of adult chickens

1992 ◽  
Vol 67 (2) ◽  
pp. 241-254 ◽  
Author(s):  
C. J. Woodbury
Keyword(s):  
Electrical Stimulation ◽  
Dorsal Horn ◽  
Single Unit ◽  
Sensory Modality ◽  
Primary Afferent ◽  
C Fibers ◽  
Multiunit Activity ◽  
Natural Stimulation ◽  
Afferent Inputs ◽  
Stimulation Of

1. The dorsal horn (DH) of chickens exhibits a novel pattern of cytoarchitectonic lamination among vertebrates, whereby lamina III lies medial, rather than ventral, to lamina II. Indeed, cutaneous nerves labeled with horseradish peroxidase (HRP) form two separate projections across the mediolateral axis of the superficial DH; each projection is somatotopically organized, such that two non-overlapping somatotopic maps are formed: the medial map within lamina III and the lateral map within lamina II. Interestingly, these two projections of cutaneous nerves are differentially labeled by HRP ligands. The present experiments were designed to address whether the separate subpopulations of cutaneous afferents, as demonstrated neuroanatomically, also differ physiologically on the basis of myelination, fiber diameter, and/or sensory modality. 2. Extracellular multi- and single-unit recordings were obtained in the DH at the ninth synsacral level of spinal adult chickens anesthetized with alpha-chloralose. Activity in lateral (laminae I/II) and medial DH (laminae III/IV) was studied after both electrical stimulation of the caudal femoral cutaneous nerve (CFC) and natural stimulation of the skin. Single units were characterized in terms of the conduction velocity (CV) and sensory modality of their cutaneous afferent inputs. 3. In multiunit recordings, electrical stimulation of the CFC above C-fiber intensities elicited a robust, long-latency response in lateral (laminae I/II) but not medial DH (laminae III/V). The afferents responsible for this late lateral response were C-fibers, as evidenced by a CV of approximately 1 m/s; birds were spinalized to rule out long spinal loops. In contrast, only a single, short-latency (and low-threshold) multiunit response was seen in medial DH, even after activation of C-fibers. 4. Natural stimulation of skin revealed a clear segregation of sensory modalities between medial (laminae III/IV) and lateral DH (laminae I/II). Innocuous mechanical stimuli were extremely effective at eliciting multiunit activity in medial DH, but ineffective in lateral DH. In contrast, noxious mechanical and thermal stimuli were extremely effective at eliciting multiunit activity in lateral DH, but were ineffective in medial DH. 5. In single-unit studies, primary afferent inputs to units in medial DH (laminae III/IV) had an average CV close to 43 m/s; no medial units received exclusive inputs from afferents with CVs less than 5.5 m/s. In contrast, primary afferent inputs to units in lateral DH (laminae I/II) had an average CV close to 10 m/s; 20% of the lateral units received exclusive inputs from C-fibers (CVs less than 1.7 m/s; N = 1.2 m/s).(ABSTRACT TRUNCATED AT 250 WORDS)

Modulation of synaptic transmission from primary afferents to spinal substantia gelatinosa neurons by group III mGluRs in GAD65-EGFP transgenic mice

2011 ◽  
Vol 105 (3) ◽  
pp. 1102-1111 ◽  
Author(s):  
Lian Cui ◽  
Yoo Rim Kim ◽  
Hye Young Kim ◽  
Seok Chan Lee ◽  
Hee-Sup Shin ◽  
...  
Keyword(s):  
Transgenic Mice ◽  
Action Potential ◽  
Synaptic Transmission ◽  
Dorsal Horn ◽  
Firing Pattern ◽  
Primary Afferents ◽  
Substantia Gelatinosa ◽  
Primary Afferent ◽  
Group Iii ◽  
Physiological Properties

Group III metabotropic glutamate receptors (mGluRs) are involved in nociceptive transmission in the spinal cord. However, the cellular mechanism underlying the modulation of synaptic transmission from nociceptive primary afferents to dorsal horn neurons by group III mGluRs has yet to be explored. In this study, we used transgenic mice expressing enhanced green fluorescent protein (EGFP) under the control of the glutamate decarboxylase (GAD) 65 promoter to identify specific subpopulations of GABAergic inhibitory interneurons. By GABA immunolabeling, we confirmed the majority of GAD65-EGFP-expressing neurons were GABAergic. Because GAD65-EGFP-expressing neurons have not been examined in detail before, we first investigated the physiological properties of GAD65-EGFP- and non-EGFP-expressing neurons in substantia gelatinosa (SG) of the spinal dorsal horn. Membrane properties, such as the resting membrane potential, membrane capacitance, action potential threshold, and action potential height, differed significantly between these two groups of neurons. Most EGFP-expressing neurons displayed a tonic firing pattern (73% of recorded neurons) and received monosynaptic Aδ and/or C primary afferent inputs (85% of recorded neurons). In contrast, we observed a delayed firing pattern in 53% of non-EGFP-expressing neurons. After identifying the physiological properties of EGFP-expressing neurons, we tested the effects of group III mGluRs on synaptic transmission pharmacologically. A group III mGluR agonist, L-AP4, attenuated Aδ fiber-evoked synaptic transmission but did not affect C fiber-evoked synaptic transmission to EGFP-expressing neurons. Similar primary afferent-specific inhibition by L-AP4 was also observed in non-EGFP-expressing neurons. Moreover, Aδ fiber-evoked synaptic transmission was suppressed by a selective mGluR7 agonist, AMN082. These results suggest that modulation of the synaptic transmission from primary afferents to SG neurons by group III mGluR agonist is specific to the type of nociceptive primary afferents but not to the type of target neurons.

Effects of Sciatic Nerve Axotomy on Excitatory Synaptic Transmission in Rat Substantia Gelatinosa

2009 ◽  
Vol 102 (6) ◽  
pp. 3203-3215 ◽  
Author(s):  
Yishen Chen ◽  
Sridhar Balasubramanyan ◽  
Aaron Y. Lai ◽  
Kathryn G. Todd ◽  
Peter A. Smith
Keyword(s):  
Sciatic Nerve ◽  
Spontaneous Activity ◽  
Dorsal Horn ◽  
Substantia Gelatinosa ◽  
Inhibitory Neurons ◽  
Resting Membrane Potential ◽  
Afferent Neurons ◽  
Primary Afferent Neurons ◽  
Primary Afferent ◽  
Synaptic Excitation

Injury or section of a peripheral nerve can promote chronic neuropathic pain. This is initiated by the appearance and persistence of ectopic spontaneous activity in primary afferent neurons that promotes a secondary, enduring increase in excitability of sensory circuits in the spinal dorsal horn (“central sensitization”). We have previously shown that 10–20 days of chronic constriction injury (CCI) of rat sciatic nerve produce a characteristic “electrophysiological signature” or pattern of changes in synaptic excitation of five different electrophysiologically defined neuronal phenotypes in the substantia gelatinosa of the dorsal horn. Although axotomy and CCI send different signals to the dorsal horn, we now find, using whole cell recording, that the “electrophysiological signature” produced 12–22 days after sciatic axotomy is quite similar to that seen with CCI. Axotomy thus has little effect on resting membrane potential, rheobase, current–voltage characteristics, or excitability of most neuron types; however, it does decrease excitatory synaptic drive to tonic firing neurons, while increasing that to delay firing neurons. Since many tonic neurons are GABAergic, whereas delay neurons do not contain γ-aminobutyric acid, axotomy may reduce synaptic excitation of inhibitory neurons while increasing that of excitatory neurons. Further analysis of spontaneous and miniature (tetrodotoxin-resistant) excitatory postsynaptic currents is consistent with the possibility that decreased excitation of tonic neurons reflects loss of presynaptic contacts. By contrast, increased excitation of “delay” neurons may reflect increased frequency of discharge of presynaptic action potentials. This would explain how synaptic excitation of tonic cells decreases despite the fact that axotomy increases spontaneous activity in primary afferent neurons.

Primary Afferent Fibers That Contribute to Increased Substance P Receptor Internalization in the Spinal Cord After Injury

1999 ◽  
Vol 81 (3) ◽  
pp. 1379-1390 ◽  
Author(s):  
Brian J. Allen ◽  
Jun Li ◽  
Patrick M. Menning ◽  
Scott D. Rogers ◽  
Joseph Ghilardi ◽  
...  
Keyword(s):  
Spinal Cord ◽  
Electrical Stimulation ◽  
Dorsal Horn ◽  
Nerve Transection ◽  
Primary Afferent ◽  
Lamina I ◽  
C Fibers ◽  
Afferent Fibers ◽  
Primary Afferent Fibers ◽  
Stimulation Of

Primary afferent fibers that contribute to increased substance P receptor internalization in the spinal cord after injury. Upon noxious stimulation, substance P (SP) is released from primary afferent fibers into the spinal cord where it interacts with the SP receptor (SPR). The SPR is located throughout the dorsal horn and undergoes endocytosis after agonist binding, which provides a spatial image of SPR-containing neurons that undergo agonist interaction. Under normal conditions, SPR internalization occurs only in SPR+ cell bodies and dendrites in the superficial dorsal horn after noxious stimulation. After nerve transection and inflammation, SPR immunoreactivity increases, and both noxious as well as nonnoxious stimulation produces SPR internalization in the superficial and deep dorsal horn. We investigated the primary afferent fibers that contribute to enhanced SPR internalization in the spinal cord after nerve transection and inflammation. Internalization evoked by electrical stimulation of the sciatic nerve was examined in untreated animals, at 14 days after sciatic nerve transection or sham surgery and at 3 days after hindpaw inflammation. Electrical stimulation was delivered at intensities to excite Aβ fibers only, Aβ and Aδ fibers or A and C fibers as determined by the compound action potential recorded from the tibial nerve. Electrical stimuli were delivered at a constant rate of 10 Hz for a duration of 5 min. Transection of the sciatic nerve and inflammation produced a 33.7 and 32.5% increase in SPR and immunoreactivity in lamina I, respectively. Under normal conditions, stimulation of Aδ or C fibers evoked internalization that was confined to the superficial dorsal horn. After transection or inflammation, there was a 20–24% increase in the proportion of SPR+ lamina I neurons that exhibited internalization evoked by stimulation of Aδ fibers. The proportion of lamina I SPR+ neurons that exhibited internalization after stimulation of C-fibers was not altered by transection or inflammation because this was nearly maximal under normal conditions. Moreover, electrical stimulation sufficient to excite C fibers evoked SPR internalization in 22% of SPR+ lamina III neurons after nerve transection and in 32–36% of SPR+ neurons in lamina III and IV after inflammation. Stimulation of Aβ fibers alone never evoked internalization in the superficial or deep dorsal horn. These results indicate that activation of small-caliber afferent fibers contributes to the enhanced SPR internalization in the spinal cord after nerve transection and inflammation and suggest that recruitment of neurons that possess the SPR contributes to hyperalgesia.

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