Morphology of A beta hair follicle afferent collaterals in dorsal horn of cats with neonatal chronic denervation of digits

1993 ◽  
Vol 70 (6) ◽  
pp. 2399-2410
Author(s):  
P. Wilson ◽  
P. J. Snow

1. The effect of neonatal denervation of two adjacent hindpaw digits (digits 3 and 4) in the cat on the morphology of spinal collaterals of identified A beta hair follicle afferents (HFAs) with receptive fields (RFs) on the neighbouring digits has been investigated using intra-axonal injection of horseradish peroxidase. 2. The morphology of collaterals of HFAs innervating intact digits (digit 2 or digit 5) was examined within the neonatally and chronically deprived region of dorsal horn by selectively injecting the afferents directly over this region. 3. Of a total of nine injected axons, seven had RFs on the distal part of digit 2, whereas two had RFs on the distal part of digit 5. With the exception of one of the digit 5 afferents, all injected afferents gave rise to stained collaterals throughout the chronically deprived digit representation. 4. Many collaterals within the chronically deprived region of dorsal horn gave rise to arborizations having relatively large numbers of boutons when compared with previously described somatotopically inappropriate (SIA) collaterals in the normal adult cat. 5. It is suggested that neonatal denervation of digits in the cat may lead to collateral sprouting and bouton formation by SIA collaterals of A beta HFAs innervating adjacent intact digits. This morphological plasticity could explain the previously reported functional reorganization of the RFs of spinocervical tract neurons that occurs in these neonatally deafferented animals.

1991 ◽  
Vol 66 (3) ◽  
pp. 762-776 ◽  
Author(s):  
P. Wilson ◽  
P. J. Snow

1. The effect of transection and ligation of the digital nerves of either one (toe 3) or two (toe 3 and toe 4) hindpaw digits, in the first postnatal week, on the tactile receptive fields (RFs) of spinocervical tract (SCT) neurons was studied in adult, alpha-chloralose-anesthetized cats. Immediately before recording, the digital nerves of the corresponding digit(s) of the opposite, intact hindpaw were transected, and the neonatally lesioned digital nerves were recut proximal to the transection neuroma. 2. In the medial part of the dorsal horn at the L6-L7 level, the digits of the hindlimb are represented in the RFs of SCT cells in a precise axial sequence from the most medial digit (toe 2) rostrally to the most lateral digit (toe 5) caudally. Acute denervation of one or two digits in the adult produced an area in the ipsilateral dorsal horn in which SCT cells lacked any RFs. When acute denervation was restricted to a single digit, the unresponsive region of dorsal horn was approximately 3 mm in length, and when two digits were denervated the unresponsive zone was approximately 6 mm long. Because the representation of the toes of the left hindpaw is a mirror image of that of the right, the rostrocaudal extent and position of the region of unresponsive SCT cells was used to assess the location of the borders of the chronically deprived region on the opposite side of the cord. 3. In all cats examined after neonatal denervation of toe 3, most (89%) of the SCT cells sampled within the chronically deprived toe 3 representation had RFs. These RFs were either on toe 2 (44%) or toe 4 (18%), and a large proportion of cells (38%) had multiple RFs with components on both toe 2 and toe 4. In most cases the cells fired briskly to displacement of hairs or light touch of the skin within these RFs. SCT cells with a RF on toe 2 and/or toe 4 were found throughout the whole 3-mm length of the chronically deprived toe 3 region, but cells with a RF on toe 2 were more commonly found than cells with a RF on toe 4 at axial distances greater than or equal to 1.5 mm from the boundary of the normal representations of the respective digit. 4. After chronic, neonatal denervation of both toe 3 and toe 4, 59% of SCT cells sampled overall had RFs, but there was a large degree of interanimal variation in the proportion of unresponsive neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1980 ◽  
Vol 43 (1) ◽  
pp. 102-117 ◽  
Author(s):  
L. M. Pubols ◽  
M. E. Goldberger

1. Collateral sprouting of L6 dorsal root afferents within the dorsal horn of the L6 spinal cord segment has been shown anatomically to occur following transection of all other lumbosacral dorsal roots in the cat. The present study was performed to examine a possible physiological correlate of that sprouting, namely, an altered somatotopic organization of the dorsal horn at L6. This was evaluated by microelectrode mapping of the L6 dorsal horn in normal cats and in cats with L6 spared, lumbosacral dorsal rhizotomies performed 2 days (subacute spared root) or more than 8 wk (chronic spared root), prior to recording. 2. In normal cats the mediolateral somatotopic sequence of hindlimb representation in the L6 dorsal horn is ventral digits 2 and 3, dorsal digits 2 and 3, dorsal foot, rostral and lateral ankle, lateral leg, lateral thigh, and back. In both subacute and chronic spared-root cats the somatotopic sequence is similar to that of normal cats, but there is a loss of proximal thigh and back representation. This proximal body region is represented at the lateral edge of the dorsal horn in normal animals. 3. There was a partial loss of responsiveness of cells in the dorsal horn in the subacute spared-root group and a partial recovery of responsiveness in the chronic group. In the subacute group punctures exhibiting no responses to tactile input tended to be clustered in the lateral dorsal horn. 4. The lateral one-fourth of the dorsal horn in each animal was analyzed in terms of the percentage of recording loci occurring within it. The percentages of recording loci having receptive fields proximal to, distal to, and spanning the middle of the thigh (proximal, distal, and intermediate RFs) were tabulated for each animal. Subacute animals had a significantly lower-than-normal overall percentage of responsive loci in the lateral dorsal horn, but chronic animals did not. The percentage of distal fields therein was not different for the normal versus the subacute group, signifying that the loss of proximal and intermediate fields was responsible for the difference in overall percentage. Chronic animals, however, had significantly more distal fields than did normals. When all fields having any distal component were compared (i.e., distal and intermediate), the difference between the chronic and normal groups did not reach significance. One possible explanation of these findings is that loci having both proximal and distal RF components are unresponsive 2 days after partial denervation, but recover responsiveness to their spared distal input over an 8-wk period. One possible mechanism mediating these changes is localized sprouting of intact, spared axons. Other mechanisms of functional recovery, such as interneuronal sprouting, denervation supersensitivity, and unmasking of latent synapses, are discussed in relation to these and other data.


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.


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.


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.


1995 ◽  
Vol 74 (5) ◽  
pp. 2065-2076 ◽  
Author(s):  
H. R. Koerber ◽  
P. B. Brown

1. To test the hypothesis that subtotal deafferentation of dorsal horn cells can stimulate plastic changes in their receptive fields (RFs), diffuse deafferentation of the cat hindlimb dorsal horn was produced by transection of L7 or L6 and L7 dorsal roots. The following single-unit cutaneous low-threshold mechanoreceptor RF properties were compared between operated and control dorsal horns: 1) distance of RF center from tips of toes, 2) RF length-width ratio; and 3) RF area. 2. In both L7 and L6-L7 rhizotomized animals there was an increased incidence of silent electrode tracks in the most deafferented portion of the hindlimb map (the foot and toe representation). In the rhizotomized L6-L7 animals, there was also an increased incidence of symmetrically placed tracks in deafferented and control dorsal horns, in which cell RFs had no mirror-symmetrical components. In addition, cells in the lateral half of the L6 and L7 dorsal horns exhibited a proximal shift in the location of their RFs. In the rhizotomized L7 animals there was a distal shift of RFs in the L5 segment at long survival times. RFs had lower length-width ratios in L5 and L6 at short survival times and in L6 at long survival times. 3. In intact preparations, dorsal horn cells normally respond to inputs via single or small numbers of low-threshold cutaneous mechanoreceptors. Because these rhizotomies do not remove all inputs from any given area of skin, the deafferentations would produce only patchy loss of input from individual receptors. Therefore observed changes cannot be accounted for entirely by loss of afferent input, suggesting that some reorganization of dorsal horn cell RFs occurred. We conclude that the threshold stimulus for plastic change is less than total deafferentation of dorsal horn cells. At least some of the mechanisms underlying these changes may be active in normal animals in the maintenance of the somatotopic map or in conditioning.


1991 ◽  
Vol 66 (3) ◽  
pp. 696-704 ◽  
Author(s):  
R. J. Millecchia ◽  
L. M. Pubols ◽  
R. V. Sonty ◽  
J. L. Culberson ◽  
W. E. Gladfelter ◽  
...  

1. Thirty-one physiologically identified primary afferent fibers were labeled intracellularly with horseradish peroxidase (HRP). 2. A computer analysis was used to determine whether the distribution of cutaneous mechanoreceptive afferent terminals varies as a function of location within the dorsal horn somatotopic map. 3. An analysis of the geometry of the projections of these afferents has shown that 1) terminal arbors have a greater mediolateral width within the region of the foot representation than lateral to it, 2) terminal arbors have larger length-to-width ratios outside the foot representation than within it, and 3) the orientation of terminal arbors near the boundary of the foot representation reflects the angle of the boundary. Previous attribution of mediolateral width variations to primary afferent type are probably in error, although there appear to be genuine variations of longitudinal extent as a function of primary afferent type. 4. Nonuniform terminal distributions represent the first of a three-component process underlying assembly of the monosynaptic portions of cell receptive fields (RFs) and the somatotopic map. The other two components consist of the elaboration of cell dendritic trees and the establishment of selective connections. 5. The variation of primary afferent terminal distributions with map location is not an absolute requirement for development of the map; for example, the RFs of postsynaptic cells could be assembled with the use of a uniform terminal distribution for all afferents, everywhere in the map, as long as cell dendrites penetrate the appropriate portions of the presynaptic neuropil and receive connections only from afferent axons contributing to their RFs.(ABSTRACT TRUNCATED AT 250 WORDS)


1989 ◽  
Vol 62 (4) ◽  
pp. 854-863 ◽  
Author(s):  
J. M. Laird ◽  
F. Cervero

1. Single-unit electrical activity has been recorded from 42 dorsal horn neurons in the sacral segments of the rat's spinal cord. The sample consisted of 20 multireceptive (class 2) cells with both A- and C-fiber inputs and 22 nocireceptive (class 3) cells. All neurons had cutaneous receptive fields (RFs) on the tail. 2. The RF sizes of the cells and their response thresholds to mechanical stimulation of the skin were determined before and after each of a series of 2-min noxious mechanical stimuli. Up to five such stimuli were delivered at intervals ranging from 10 to 60 min. In most cases, only one cell per animal was tested. 3. The majority of neurons were tested in barbiturate-anesthetized animals. However, to test whether or not this anesthetic influenced the results obtained, experiments were also performed in halothane-anesthetized and decerebrate-spinal preparations. The results from these experiments are considered separately. 4. All of the neurons responded vigorously to the first noxious pinch stimulus and all but one to the rest of the stimuli in the series. The responses of the neurons varied from stimulus to stimulus, but there were no detectable trends in the two groups of cells. 5. The RFs of the class 2 cells showed large increases (624.3 +/- 175.8 mm2, mean +/- SE) after the application of the pinch stimuli. The RFs of the class 3 neurons, which were initially smaller than those of the class 2 cells, either did not increase in size or showed very small increases after the pinch stimuli (38.3 +/- 11.95 mm2, mean +/- SE). 6. Some cells in both groups (6/10 class 2 cells and 7/16 class 3 cells) showed a decrease in mechanical threshold as a result of the noxious mechanical stimulus, but none of the class 3 cells' thresholds dropped below 20 mN into the low-threshold range. 7. The results obtained in the halothane-anesthetized and decerebrate-spinal animals were very similar to those seen in the barbiturate-anesthetized experiments, with the exception that in the decerebrate-spinal animals, the RFs of the class 2 cells were initially larger and showed only small increases.(ABSTRACT TRUNCATED AT 400 WORDS)


2001 ◽  
Vol 86 (6) ◽  
pp. 2868-2877 ◽  
Author(s):  
Koichi Iwata ◽  
Takao Imai ◽  
Yoshiyuki Tsuboi ◽  
Akimasa Tashiro ◽  
Akiko Ogawa ◽  
...  

The effects of inferior alveolar nerve (IAN) transection on escape behavior and MDH neuronal activity to noxious and nonnoxious stimulation of the face were precisely analyzed. Relative thresholds for escape from mechanical stimulation applied to the whisker pad area ipsilateral to the transection were significantly lower than that for the contralateral and sham-operated whisker pad until 28 days after the transection, then returned to the preoperative level at 40 days after transection. A total of 540 neurons were recorded from the medullary dorsal horn (MDH) of the nontreated naive rats [low-threshold mechanoreceptive (LTM), 27; wide dynamic range (WDR), 31; nociceptive specific (NS), 11] and sham-operated rats with skin incision (LTM, 34; WDR, 30; NS, 23) and from the ipsilateral (LTM, 82; WDR, 82; NS, 31) and contralateral MDH relative to the IAN transection (LTM, 77; WDR, 82; NS, 33). The electrophysiological properties of these neurons were precisely analyzed. Background activity of WDR neurons on the ipsilateral side relative to the transection was significantly increased at 2–14 days after the operation as compared with that of naive rats. Innocuous and noxious mechanical-evoked responses of LTM and WDR neurons were significantly enhanced at 2–14 days after IAN transection. The mean area of the receptive fields of WDR neurons was significantly larger on the ipsilateral MDH at 2–7 days after transection than that of naive rats. We could not observe any modulation of thermal responses of WDR and NS neurons following IAN transection. Also, no MDH neurons were significantly affected in the rats with sham operations. The present findings suggest that the increment of neuronal activity of WDR neurons in the MDH following IAN transection may play an important role in the development of the mechano-allodynia induced in the area adjacent to the area innervated by the injured nerve.


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