Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents

1986 ◽  
Vol 55 (6) ◽  
pp. 1153-1186 ◽  
Author(s):  
M. F. Jacquin ◽  
W. E. Renehan ◽  
R. D. Mooney ◽  
R. W. Rhoades

Intracellular recording and horseradish peroxidase (HRP) labeling were used to examine structure-function relationships in the medullary dorsal horn (MDH) and rostral cervical dorsal horn. In Nembutal-anesthetized rats, 78 trigeminal (V) primary afferent fibers were physiologically characterized and injected with HRP. Axons were sufficiently well stained to reconstruct all of their collaterals in the MDH. Many also extended into the cervical dorsal horn. Except for four axons, which responded best to noxious stimuli, all responded at short (mean = 0.50 ms) latencies to V ganglion shocks and to innocuous stimulation. Forty-five of our recovered fibers were associated with facial vibrissae and responded in either a rapidly adapting, slowly adapting type I, slowly adapting type IIa, or slowly adapting type IIb fashion. The adequate stimuli consisted of either slow deflection, high-velocity deflection, or a noxious pinch of the vibrissa follicle. The collaterals of all of the above-described mystacial vibrissa primary afferents proceeded directly to their region of arborization in a plane perpendicular to the lateral border of the medulla to collectively form a largely continuous, circumscribed terminal column. This longitudinally oriented column of terminal and en passant boutons angled from lamina V rostrally to lamina III caudally. In the magnocellular laminae of the MDH, all mystacial vibrissa primary afferents gave rise to similarly shaped arbors, regardless of their functional classification. While morphological variability was observed both within and between individual axons, variance between functional classes was no greater than that within a class. Moreover, number of collaterals, number of boutons, or bouton size did not distinguish functional classes. Nonmystacial vibrissa afferent arbors, with more caudal peripheral fields, had their primary arbor focus in C1 and C2 dorsal horn. These arbors had relatively little rostrocaudal overlap with mystacial vibrissa afferents, though they exhibited the same lamina V-to-III shift as they descended through the cervical cord. Unlike mystacial vibrissa afferents in the MDH, their collaterals followed a tortuous course and often occupied laminae II-V in one transverse section. The relative location of each vibrissa afferent's terminal field could be predicted by the particular vibrissa innervated. Dorsal vibrissae afferents had ventrolateral terminations and ventral vibrissae afferents terminated dorsomedially. Rostral vibrissae were represented in the rostral MDH, whereas caudal vibrissae were represented in the caudal MDH and rostral cervical dorsal horn.(ABSTRACT TRUNCATED AT 400 WORDS)

1999 ◽  
Vol 81 (4) ◽  
pp. 1636-1644 ◽  
Author(s):  
H. Richard Koerber ◽  
Karoly Mirnics ◽  
Anahid M. Kavookjian ◽  
Alan R. Light

Ultrastructural analysis of ectopic synaptic boutons arising from peripherally regenerated primary afferent fibers. The central axons of peripherally regenerated Aβ primary sensory neurons were impaled in the dorsal columns of α-chloralose-anesthetized cats 9–12 mo after axotomy. The adequate peripheral stimulus was determined, and the afferent fibers intracellularly stimulated while simultaneously recording the resulting cord dorsum potentials (CDPs). Fibers that successfully had reinnervated the skin responded to light tactile stimulation, and evoked CDPs that suggested dorsally located boutons were stained intracellularly with horseradish peroxidase (HRP). Two HRP-stained regenerated Aβ afferent fibers were recovered that supported large numbers of axon collaterals and swellings in laminae I, IIo, and IIi. Sections containing the ectopic collateral fibers and terminals in the superficial dorsal horn were embedded in plastic. Analyses of serial ultrathin sections revealed that ectopic projections from both regenerated fibers supported numerous synaptic boutons filled with clear round vesicles, a few large dense core vesicles (LDCVs) and several mitochondria (>3). All profiles examined in serial sections (19) formed one to three asymmetric axo-dendritic contacts. Unmyelinated portions of ectopic fibers giving rise to en passant and terminal boutons often contained numerous clear round vesicles. Several boutons (47%) received asymmetric contacts from axon terminals containing pleomorphic vesicles. These results strongly suggest that regenerated Aβ fibers activated by light tactile stimuli support functional connections in the superficial dorsal horn that have distinct ultrastructural features. In addition, the appearance of LDCVs suggests that primary sensory neurons are capable of changing their neurochemical phenotype.


2002 ◽  
Vol 87 (2) ◽  
pp. 732-739 ◽  
Author(s):  
Guo-Du Wang ◽  
Min Zhuo

Glutamate is the major excitatory amino acid neurotransmitter in the CNS, including the neocortex, hippocampus, and spinal cord. Normal synaptic transmission is mainly mediated by glutamate AMPA and/or kainate receptors. Glutamate N-methyl-d-aspartate (NMDA) receptors are normally inactive and only activated when a sufficient postsynaptic depolarization is induced by the activity. Here we show that in sensory synapses of adult mouse, some synaptic responses (26.3% of a total of 38 experiments) between primary afferent fibers and dorsal horn neurons are almost completely mediated by NMDA receptors. Dorsal root stimulation did not elicit any detectable AMPA/kainate receptor-mediated responses in these synapses. Unlike young spinal cord, serotonin alone did not produce any long-lasting synaptic enhancement in adult spinal dorsal horn neurons. However, co-application of the adenylyl cyclase activator forskolin and serotonin (5-HT) produced long-lasting enhancement, including the recruitment of functional AMPA receptor-mediated responses. Calcium-sensitive, calmodulin-regulated adenylyl cyclases (AC1, AC8) are required for the enhancement. Furthermore the thresholds for generating action potential responses were decreased, and, in many cases, co-application of forskolin and 5-HT led to the generation of action potentials by previously subthreshold stimulation of primary afferent fibers in the presence of the NMDA receptor blocker 2-amino-5-phosphonovaleric acid. Our results suggest that pure NMDA synapses exist on sensory neurons in adult spinal cord and that they may contribute to functional sensory transmission. The synergistic recruitment of functional AMPA responses by 5-HT and forskolin provides a new cellular mechanism for glutamatergic synapses in mammalian spinal cord.


2001 ◽  
Vol 85 (5) ◽  
pp. 1793-1804 ◽  
Author(s):  
G. T. Coleman ◽  
H. Bahramali ◽  
H. Q. Zhang ◽  
M. J. Rowe

The marmoset monkey, Callithrix jacchus, has increasingly been the subject of experiments for the analysis of somatosensory system function in simian primates. However, as response properties of the mechanoreceptive afferent fibers supplying the skin have not been characterized for this primate, the present study was undertaken to classify fibers innervating the glabrous skin of the marmoset hand and determine whether they resembled those described for other mammalian species, including cat, macaque monkey, and human subjects. Forty-seven tactile afferent fibers with receptive fields (RFs) on the glabrous skin of the hand were isolated in fine median and ulnar nerve strands. Controlled tactile stimuli, including static indentation and skin vibration, were used to classify fibers. Twenty-six (55%) responded to static indentation in a sustained manner and were designated slowly adapting (SA) fibers, while 21 (45%) were selectively sensitive to the dynamic components of the stimulus. The SA fibers had well-defined boundaries to their RFs, lacked spontaneous activity in most cases (23/26 fibers), had an irregular pattern of discharge to static skin indentation, and displayed graded response levels as a function of indentation amplitude, attributes that were consistent with the properties of slowly adapting type I (SAI) fibers described in other species. The dynamically sensitive afferent fibers could be subdivided into two distinct functional classes, based on their responses to vibrotactile stimulation. The majority (15/21) responded best to lower frequency vibration (∼10–50 Hz) and had small RFs, whereas the second class responded preferentially to higher frequency vibration (50–700 Hz) with maximal sensitivity at ∼200–300 Hz. These two classes resembled, respectively, the rapidly adapting (RA) and Pacinian corpuscle–related (PC) fiber classes found in other species, and like them, responded to vibration with tightly phase-locked patterns of response over a wide range of frequencies. The results demonstrate that the functional classes of tactile afferent fibers that supply the glabrous skin in the marmoset monkey appear to correspond with those described previously for the cat and macaque monkey, and are similar to those supplying the human hand and fingers, although the SA fibers in the human hand appear to fall into two classes, the SAI and SAII fibers. With the increasing use of the marmoset monkey as a primate model for somatosensory system studies, these data now allow tactile neurons identified at central locations, such as the cerebral cortex and thalamus, to be classified in relation to inputs from the peripheral classes identified in the present study.


2021 ◽  
Vol 22 (1) ◽  
pp. 414
Author(s):  
Antonella Comitato ◽  
Rita Bardoni

Sensory primary afferent fibers, conveying touch, pain, itch, and proprioception, synapse onto spinal cord dorsal horn neurons. Primary afferent central terminals express a wide variety of receptors that modulate glutamate and peptide release. Regulation of the amount and timing of neurotransmitter release critically affects the integration of postsynaptic responses and the coding of sensory information. The role of GABA (γ-aminobutyric acid) receptors expressed on afferent central terminals is particularly important in sensory processing, both in physiological conditions and in sensitized states induced by chronic pain. During the last decade, techniques of opto- and chemogenetic stimulation and neuronal selective labeling have provided interesting insights on this topic. This review focused on the recent advances about the modulatory effects of presynaptic GABAergic receptors in spinal cord dorsal horn and the neural circuits involved in these mechanisms.


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