Intraaxonal injection of neurobiotin reveals the long-ranging projections of A beta-hair follicle afferent fibers to the cat dorsal horn

1996 ◽  
Vol 76 (1) ◽  
pp. 242-254 ◽  
Author(s):  
P. Wilson ◽  
P. D. Kitchener ◽  
P. J. Snow

1. The morphology and somatotopic organization of the spinal arborizations of identified A beta-hair follicle afferent fibers (HFAs) with receptive fields (RFs) on the digits have been investigated in the cat by the use of intraaxonal injection of the tracer n-(2 aminoethyl) biotinamide. 2. In three cats, the long-ranging projections of six HFAs were examined by selectively injecting afferents with RFs on digit 2, 4, or 5, directly over the digit 3 representation, and examining their collateral morphology in transverse sections of the spinal cord. The rostral and caudal boundaries of the digit 3 representation were determined by mapping the RFs of identified spinocervical tract (SCT) neurons. 3. In two more cats, three HFAs were injected at random rostrocaudal positions and their morphology was examined in parasagittal sections. In one animal (2 HFAs), the somatotopy of the digit representation was again determined by mapping the RFs of SCT neurons. In the remaining cat (1 HFA), the somatotopy of the dorsal horn was mapped from the RFs of unidentified dorsal horn neurons. 4. Hair follicle afferents emitted many more collaterals, over much greater rostrocaudal distances, than indicated by previous horseradish peroxidase studies, and all collaterals gave rise to synaptic boutons. 5. HFAs that have RFs confined to a small part of a digit give rise to bouton-bearing axonal branches throughout the entire rostrocaudal extent of the hindpaw representation.

1986 ◽  
Vol 56 (4) ◽  
pp. 1022-1038 ◽  
Author(s):  
D. E. Meyers ◽  
P. J. Snow

Single-unit spike-triggered averaging has been used to study the distribution of activity in the central processes of 11 single hair follicle afferent (HFA) fibers in relation to the somatotopic organization of dorsal horn neurons (DHNs). Central responses could be recorded from all but one HFA, and the waveforms of these responses were similar to the biphasic, monophasic positive and compound terminal potentials (TPs), the triphasic, positive-negative-positive axonal (preterminal) potentials (APs), and the focal synaptic potentials (FSPs) described by other workers in different preparations. No central responses could be recorded from one HFA even though this axon was shown to be intact throughout the experiment and noise levels in the averaged records were below 3.1 microV. The spatial organization of TPs and APs mirrored the anatomical organization determined using intraaxonal staining only in that the region containing these potentials was a longitudinally orientated narrow (mean width = 405 microns) strip of dorsal horn. Within this strip large TPs, APs, and FSPs were usually found only in those regions in which the receptive field (RF) of the HFA was relatively central to the RFs of DHNs. The region in which the RFs of DHNs encompassed the RF of the HFA, the somatotopically appropriate region, was also organized into a longitudinally orientated strip of dorsal horn of approximately the same width as the strip containing TPs and APs. In any single experiment the strips formed by the somatotopically appropriate region and the TP-AP region occupied the same mediolateral position, but in contrast, the rostral and/or caudal boundaries of these strips often occurred at different levels along the dorsal horn. In some cases the TP-AP strip extended rostrally and/or caudally beyond the somatotopically appropriate region or ended at the same rostrocaudal level. In other cases the somatotopically appropriate region extended rostrally and/or caudally beyond the TP-AP strip. These results are discussed in relation to the rostrocaudal spread of the dendritic trees and the RF organization of DHNs. The results show clearly that in intact cats, anesthetized with alpha-chloralose, some HFAs give rise to collaterals in somatotopically inappropriate regions of the dorsal horn and that at least some parts of these collaterals are invaded by incoming action potentials. The question of whether some HFAs give rise to collaterals that are either infrequently invaded or not invaded at all is discussed.


2008 ◽  
Vol 99 (6) ◽  
pp. 3144-3150 ◽  
Author(s):  
Rachel A. Ingram ◽  
Maria Fitzgerald ◽  
Mark L. Baccei

The lower thresholds and increased excitability of dorsal horn neurons in the neonatal rat suggest that inhibitory processing is less efficient in the immature spinal cord. This is unlikely to be explained by an absence of functional GABAergic inhibition because antagonism of γ-aminobutyric acid (GABA) type A receptors augments neuronal firing in vivo from the first days of life. However, it is possible that more subtle deficits in GABAergic signaling exist in the neonate, such as decreased reliability of transmission or greater depression during repetitive stimulation, both of which could influence the relative excitability of the immature spinal cord. To address this issue we examined monosynaptic GABAergic inputs onto superficial dorsal horn neurons using whole cell patch-clamp recordings made in spinal cord slices at a range of postnatal ages (P3, P10, and P21). The amplitudes of evoked inhibitory postsynaptic currents (IPSCs) were significantly lower and showed greater variability in younger animals, suggesting a lower fidelity of GABAergic signaling at early postnatal ages. Paired-pulse ratios were similar throughout the postnatal period, whereas trains of stimuli (1, 5, 10, and 20 Hz) revealed frequency-dependent short-term depression (STD) of IPSCs at all ages. Although the magnitude of STD did not differ between ages, the recovery from depression was significantly slower at immature GABAergic synapses. These properties may affect the integration of synaptic inputs within developing superficial dorsal horn neurons and thus contribute to their larger receptive fields and enhanced afterdischarge.


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.


1982 ◽  
Vol 48 (2) ◽  
pp. 481-489 ◽  
Author(s):  
H. R. Koerber ◽  
P. B. Brown

1. The dorsal horn lamina III-IV projections of 10 hindlimb nerves innervating most of the hindlimb have been studied in the cat using transganglionic transport of horseradish peroxidase (HRP). The somatotopic organization of whole cutaneous nerve projections was largely in register with the somatotopic organization of dorsal horn cells. That is, nerves projected to areas of dorsal horn where their innervation fields overlap the receptive fields of dorsal horn cells. 2. However, long-ranging projections were observed that were more extensive than predicted from the somatotopy of dorsal horn cells: these long-ranging projections may reflect the presence of normally ineffective synapses (synapses that do not cause postsynaptic discharge during receptive-field mapping of dorsal horn cells,) or a misconception of dorsal horn cell somatotopy in S2 and caudal segments, or the existence of a functionally separate cell group in ventral lamina IV and lamina V of these segments. 3. The cutaneous innervation fields of homologous nerves possessed high bilateral symmetry, as did their lamina III-IV projection fields. The degree of separation or overlap of two cutaneous nerves' projection fields was predictable from the degree of separation or overlap of their cutaneous innervation fields.


1987 ◽  
Vol 57 (3) ◽  
pp. 803-818 ◽  
Author(s):  
P. Wilson ◽  
P. J. Snow

The effect of acute and chronic section of the digital nerves of a single toe on the organization of low-threshold, mechanoreceptive fields of lumbosacral spinocervical tract (SCT) neurons has been studied in adult cats anesthetized with chloralose. The immediate effect of sectioning the digital nerves of a single toe is to produce a patch of dorsal horn in the medial region of the ipsilateral lumbosacral cord in which SCT neurons lack any peripheral receptive field when gentle hair movement or light touch of glabrous skin are used as stimuli. Other SCT neurons in the region may lose only part of their receptive fields. Between 30 and 70 days later most of the affected SCT neurons have established receptive fields. These are mainly on somatotopically inappropriate areas of skin medially and laterally adjacent to the denervated region. A small proportion of SCT neurons form discontinuous receptive fields. The relative somatotopic organization within the affected region remains unchanged. As there is no sign of regeneration of the sectioned nerves the new receptive fields must result from a central reorganization of excitatory inputs to SCT neurons. It is concluded that chronic peripheral nerve section affects the anatomical and physiological mechanisms underlying the formation of light touch receptive fields of dorsal horn neurons in the lumbosacral cord of the adult cat, but that the resulting reorganization of receptive fields is spatially restricted.


1998 ◽  
Vol 80 (1) ◽  
pp. 120-129 ◽  
Author(s):  
Robert W. Dykes ◽  
A. D. Craig

Dykes, Robert W. and A. D. Craig. Control of size and excitability of mechanosensory receptive fields in dorsal column nuclei by homolateral dorsal horn neurons. J. Neurophysiol. 80: 120–129 1998. Both accidental and experimental lesions of the spinal cord suggest that neuronal processes occurring in the spinal cord modify the relay of information through the dorsal column-lemniscal pathway. How such interactions might occur has not been adequately explained. To address this issue, the receptive fields of mechanosensory neurons of the dorsal column nuclei were studied before and after manipulation of the spinal dorsal horn. After either a cervical or lumbar laminectomy and exposure of the dorsal column nuclei in anesthetized cats, the representation of the hindlimb or of the forelimb was defined by multiunit recordings in both the dorsal column nuclei and in the ipsilateral spinal cord. Next, a single cell was isolated in the dorsal column nuclei, and its receptive field carefully defined. Each cell could be activated by light mechanical stimuli from a well-defined cutaneous receptive field. Generally the adequate stimulus was movement of a few hairs or rapid skin indentation. Subsequently a pipette containing either lidocaine or cobalt chloride was lowered into the ipsilateral dorsal horn at the site in the somatosensory representation in the spinal cord corresponding to the receptive field of the neuron isolated in the dorsal column nuclei. Injection of several hundred nanoliters of either lidocaine or cobalt chloride into the dorsal horn produced an enlargement of the receptive field of the neuron being studied in the dorsal column nuclei. The experiment was repeated 16 times, and receptive field enlargements of 147–563% were observed in 15 cases. These data suggest that the dorsal horn exerts a tonic inhibitory control on the mechanosensory signals relayed through the dorsal column-lemniscal pathway. Because published data from other laboratories have shown that receptive field size is controlled by signals arising from the skin, we infer that the control of neuronal excitability, receptive field size and location for lemniscal neurons is determined by tonic afferent activity that is relayed through a synapse in the dorsal horn. This influence of dorsal horn neurons on the relay of mechanosensory information through the lemniscal pathways must modify our traditional views concerning the relative independence of these two systems.


1986 ◽  
Vol 55 (3) ◽  
pp. 604-617 ◽  
Author(s):  
P. Wilson ◽  
D. E. Meyers ◽  
P. J. Snow

The somatotopic organization of spinocervical tract cells and unidentified dorsal horn neurons that lie in the same depth range as the spinocervical tract cells has been examined in detail in the lumbosacral enlargement of cats anesthetized with alpha-chloralose. Only gentle hair movement or light touch of glabrous skin were used as stimuli. Within the region of the dorsal horn containing these neurons there is a precise somatotopic organization. However, there is considerable variation between animals in the relationship between the somatotopic map and the lumbosacral segmental boundaries. The somatotopic map described here is considered to be restricted to a 300- to 500-micron thick lamina. In the medial half to two-thirds of this lamina in the L6 and L7 segments the toes are represented in a rostrocaudal sequence from toe 2 to toe 5. Over the most medial 200-500 micron of this part of the dorsal horn are found cells that respond to stimulation of the glabrous skin of the toe pads and the central pad. The toe representation is surrounded by a strip of foot representation, which is in turn surrounded by a strip of leg representation. The most lateral part of the lamina curves ventrally in the L6 and L7 segments and contains a continuous rostrocaudal representation of the skin of the thigh. In this region are found both spinocervical tract cells and unidentified dorsal horn neurons with receptive fields on the thigh. The skin of the hindlimb is represented such that a line of discontinuity runs down the posteromedial thigh, leg, and foot. Skin lateral to this line is represented caudally, while skin medial to it is represented rostrally.


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