Intracellular staining study of the feline cuneate nucleus. I. Terminal patterns of primary afferent fibers

1986 ◽  
Vol 56 (5) ◽  
pp. 1268-1283 ◽  
Author(s):  
R. E. Fyffe ◽  
S. S. Cheema ◽  
A. Rustioni

The terminal arborizations of single identified cutaneous hair follicle and slowly adapting type I receptors and muscle (Ia) afferents have been studied in the cuneate nucleus of cats after intra-axonal injection of horseradish peroxidase. Penetrations were mainly at the middle and caudal levels of the nucleus--i.e., from obex to approximately 7 mm caudal to it. Following histochemical processing, the injected axons, along with their collateral branches and synaptic terminals, were visualized and examined with light and electron microscopy. Cutaneous afferents in middle cuneate (from obex to approximately 4 mm caudal to it) issued collateral branches, along the rostrocaudal axis of the nucleus, at intervals between 100 and 1,000 microns. The terminal field of each collateral's branches encompassed an area elongated largely rostrocaudally and virtually confined to the dorsal part of the middle cuneate. Although adjacent collaterals had nonoverlapping terminal arborizations, each one could give rise to separate foci of terminations. Muscle afferents differed, on the whole, from cutaneous afferents in the location and extent of collateral branching and terminal arborizations. However, because muscle fibers terminated primarily in the ventral region of the cuneate, but nevertheless exhibited sparser terminations in the dorsal part of the middle cuneate, there was some spatial overlap between zones of muscle and cutaneous projection. Synaptic boutons of cutaneous afferent fibers contained round clear vesicles, contacted dendritic profiles (sometimes more than one), and were postsynaptic to small boutons containing polymorphic vesicles. In contrast, boutons of muscle afferent fibers contacted somatic and dendritic profiles and were not postsynaptic to other boutons. The results are in general agreement with previous anatomical and electrophysiological work; however, the extent of the terminal field of single collateral branches may provide for a greater convergence of different receptor classes and of receptive fields on neurons in the middle cuneate than estimated by previous electrophysiological investigations.

1991 ◽  
Vol 66 (6) ◽  
pp. 2155-2158 ◽  
Author(s):  
R. D. Johnson ◽  
J. B. Munson

1. In cats, we studied the physiological properties of regenerating sprouts of muscle afferent fibers and compared them with sprouts from cutaneous afferent fibers. 2. Muscle nerves to the triceps surae and cutaneous sural nerves were axotomized in the popliteal fossa, and the proximal ends were inserted into nerve cuffs. Six days later, we recorded action potentials from single Groups I and II muscle and mostly Group II cutaneous afferents driven by mechanostimulation of the cuff. 3. Most muscle afferent sprouts (91%) had a regular slowly adapting discharge in response to sustained mechanical displacement of the cuff, particularly to sustained stretch stimuli, whereas most cutaneous afferents (92%) did not. Muscle afferents were more likely to have a spontaneous discharge and afterdischarge. 4. Group II muscle afferent sprouts had lower stretch thresholds and a higher incidence of spontaneous discharge compared with Group I fiber sprouts, whereas Group I fibers had a higher incidence of high-frequency afterdischarge to mechanical stimuli. 5. We conclude that, 6 days after axotomy, regenerating sprouts of muscle afferents, particularly Group II afferents, have become mechanosensitive in the absence of a receptor target and exhibit physiological properties similar to those found when innervating their native muscle but significantly different from sprouts of cutaneous afferents. Expression of these native muscle afferent firing patterns after the inappropriate reinnervation of hairy skin may be due to inherent properties of the muscle afferent fiber.


1995 ◽  
Vol 73 (2) ◽  
pp. 651-661 ◽  
Author(s):  
R. D. Johnson ◽  
J. S. Taylor ◽  
L. M. Mendell ◽  
J. B. Munson

1. In this study we investigate the peripheral receptive field properties and spinal cord connections of low-threshold muscle afferent fibers cross-regenerated into the skin to determine whether a cutaneous target can rescue physiological functions lost after chronic axotomy. 2. In adult cats the medial gastrocnemius (MG) muscle nerve was coated with the distal cut end of either the caudal or lateral cutaneous sural nerves and allowed to regenerate into the hairy skin (postoperative period 6-30 mo). During terminal acute experiments we made recordings of single MG afferent fibers in dorsal root filaments and peripheral nerve. Conduction velocity and receptive field characteristics were determined for each fiber. In addition, the MG nerve was stimulated to elicit cord dorsum potentials and monosynaptic excitatory postsynaptic potentials (EPSPs) in heteronymous motoneurons. As controls, studies were carried out after MG nerve axotomy (postoperative period 2.5-12 mo). 3. After innervation of the skin, MG muscle afferent fibers exhibited firing characteristics and proximal segment conduction velocities like those of normal MG afferents. Responses to skin and hair stimulation consisted primarily of slowly adapting, stretch-sensitive, and steady discharge patterns, all common in normal muscle afferents but not in cutaneous afferents. These properties were observed despite the innervation of touch domes and single hairs, suggesting that the peripheral physiology of muscle afferents is a function of the axonal membrane and is not respecified by a cutaneous target and/or receptors. 4. Cord dorsum potentials were characteristic of those elicited by intact muscle afferents rather than skin afferents and showed recovery of configurations lost after chronic axotomy. 5. The monosynaptic EPSPs elicited in lateral gastrocnemius-soleus motoneurons also recovered from the reduction in amplitude observed after chronic axotomy. The configurations of these EPSPs were characteristic of muscle afferents rather than skin afferents. 6. These experiments demonstrate that the peripheral and central physiological properties of muscle afferents are rescued from the axotomy state if the afferents are allowed to reinnervate skin. We found no evidence that respecification had occurred to bring the function of muscle afferents into accord with the new cutaneous target.


1986 ◽  
Vol 55 (1) ◽  
pp. 76-96 ◽  
Author(s):  
R. P. Yezierski ◽  
R. H. Schwartz

Recordings were made from 90 identified spinomesencephalic tract (SMT) cells in the lumbosacral spinal cord of cats anesthetized with alpha-chloralose and pentobarbital sodium. Recording sites were located in laminae I-VIII. Antidromic stimulation sites were located in different regions of the rostral and caudal midbrain including the periaqueductal gray, midbrain reticular formation, and the deep layers of the superior colliculus. Twelve SMT cells were antidromically activated from more than one midbrain level or from sites in the medial thalamus. The mean conduction velocity for the population of cells sampled was 45.2 +/- 21.4 m/s. Cells were categorized based on their responses to graded intensities of mechanical stimuli and the location of excitatory and/or inhibitory receptive fields. Four major categories of cells were encountered: wide dynamic range (WDR); high threshold (HT); deep/tap; and nonresponsive. WDR and HT cells had excitatory and/or inhibitory receptive fields restricted to the ipsilateral hindlimb or extending to other parts of the body including the tail, forelimbs, and face. Some cells had long afterdischarges following noxious stimulation, whereas others had high rates of background activity that was depressed by nonnoxious and noxious stimuli. Deep/tap cells received convergent input from muscle, joint, or visceral primary afferent fibers. The placement of mechanical lesions at different rostrocaudal levels of the cervical spinal cord provided information related to the spinal trajectory of SMT axons. Six axons were located contralateral to the recording electrode in the ventrolateral/medial or lateral funiculi while two were located in the ventrolateral funiculus of the ipsilateral spinal cord. Stimulation at sites used to antidromically activate SMT cells resulted in the inhibition of background and evoked responses for 22 of 25 cells tested. Inhibitory effects were observed on responses evoked by low/high intensity cutaneous stimuli and by the activation of joint or muscle primary afferent fibers. Based on the response and receptive-field properties of SMT cells it is suggested that the SMT may have an important role in somatosensory mechanisms, particularly those related to nociception.


2003 ◽  
Vol 89 (1) ◽  
pp. 40-56 ◽  
Author(s):  
Brandon S. Minnery ◽  
Daniel J. Simons

Nucleus principalis (PrV) of the brain stem trigeminal complex mediates the processing and transfer of low-threshold mechanoreceptor input en route to the ventroposterior medial nucleus of the thalamus (VPM). In rats, this includes tactile information relayed from the large facial whiskers via primary afferent fibers originating in the trigeminal ganglion (NV). Here we describe the responses of antidromically identified VPM-projecting PrV neurons ( n = 72) to controlled ramp-and-hold deflections of whiskers. For comparison, we also recorded the responses of 64 NV neurons under identical experimental and stimulus conditions. Both PrV and NV neurons responded transiently to stimulus onset (on) and offset (off), and the majority of both populations also displayed sustained, or tonic, responses throughout the plateau phase of the stimulus (75% of NV cells and 93% of PrV cells). Averageon and off response magnitudes were similar between the two populations. In both NV and PrV, cells were highly sensitive to the direction of whisker deflection. Directional tuning was slightly but significantly greater in NV, suggesting that PrV neurons integrate inputs from NV cells differing in their preferred directions. Receptive fields of PrV neurons were typically dominated by a “principal” whisker (PW), whose evoked responses were on average threefold larger than those elicited by any given adjacent whisker (AW; n = 197). However, of the 65 PrV cells for which data from at least two AWs were obtained, most (89%) displayed statistically significanton responses to deflections of one or more AWs. AW response latencies were 2.7 ± 3.8 (SD) ms longer than those of their corresponding PWs, with an inner quartile latency difference of 1–4 ms (±25% of median). The range in latency differences suggests that some adjacent whisker responses arise within PrV itself, whereas others have a longer, multi-synaptic origin, possibly via the spinal trigeminal nucleus. Overall, our findings reveal that the stimulus features encoded by primary afferent neurons are reflected in the responses of VPM-projecting PrV neurons, and that significant convergence of information from multiple whiskers occurs at the first synaptic station in the whisker-to-barrel pathway.


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)


1994 ◽  
Vol 71 (2) ◽  
pp. 753-760 ◽  
Author(s):  
J. G. Pickar ◽  
J. M. Hill ◽  
M. P. Kaufman

1. In decerebrate cats, we investigated the responses of group III muscle afferents to dynamic exercise. The cats performed low intensity dynamic exercise on a treadmill. Group III afferent activity from the dynamically exercising triceps surae muscles was recorded from L7-S1 dorsal root filaments. 2. Single-unit recordings were obtained from 15 group III afferent fibers whose receptive fields were in the triceps surae muscles and from one group III afferent whose receptive field was in the flexor digitorum longus muscle. Conduction velocities for the 16 group III afferents ranged from 3.0 to 27.9 m/s (15.6 +/- 1.9 m/s, mean +/- SE). 3. Ten of 16 group III muscle afferents were stimulated by dynamic exercise. Of the 10, 7 were strongly responsive and 3 were mildly responsive to dynamic exercise. Each of the 10 afferents displayed at least some activity that was synchronized to the contraction phase of the step cycle. The mean developed tensions for strongly responsive afferents, mildly responsive afferents, and afferents that did not respond were 0.8 +/- 0.3, 1.3 +/- 0.5, and 0.7 +/- 0.3 Kg, respectively (P > 0.05). Thus differences in the responsiveness of the afferents to exercise were not attributable to differences in developed tensions. 4. The group III afferents that were strongly responsive to dynamic exercise were also mechanically sensitive. Each strongly responsive afferent (n = 7) was stimulated by nonnoxious pressure applied to its receptive field. Most strongly responsive afferents (n = 5) were stimulated by stretch of the triceps surae muscles.(ABSTRACT TRUNCATED AT 250 WORDS)


1993 ◽  
Vol 69 (1) ◽  
pp. 174-186 ◽  
Author(s):  
F. M. Boissonade ◽  
B. Matthews

1. Cats were prepared for chronic recording from neurons in pars oralis and pars interpolaris of the trigeminal spinal nucleus. Electrodes were implanted into canine teeth for electrical stimulation and the digastric muscle for recording electromyograms. 2. Recordings were made from the animals when they were awake and unrestrained as well as when they were lightly anesthetized. Some neurons were studied under both conditions. 3. In an awake animal, single tooth-pulp stimuli of 0.1 ms duration and < or = 1 mA intensity produced no aversive behavior. 4. The response of trigeminal brain stem neurons in the awake animal to such stimuli consisted of short (approximately 3 ms)- and long (approximately 25 ms)-latency discharges whose thresholds suggested that they were both due to inputs from fast conducting primary afferent fibers. 5. Light anesthesia reduced the number of impulses in both components and in most cases completely abolished the long-latency component evoked by low-intensity stimuli. The threshold of the short-latency component was little affected by light anesthesia. It is postulated that the short-latency component is mediated by a monosynaptic input from primary afferent fibers and the long-latency component by a polysynaptic input from these same fibers. 6. All neurons that responded to tooth-pulp stimulation had inputs from other orofacial sites both in the awake and lightly anesthetized states. After light anesthesia, these receptive fields were altered in only 3 out of 15 neurons. 7. The majority of neurons (18 out of 20) were not spontaneously active in the awake animal. Spontaneous activity in the other two was reduced by light anesthesia. 8. The threshold of the digastric reflex evoked by tooth-pulp stimulation was not altered by light anesthesia, but the size of the response was reduced. 9. The effects of changing the level of anesthesia from deep to light (i.e., without and with reflex withdrawal to squeezing a paw) on the responses to tooth-pulp stimulation were also studied. Decreasing the anesthetic depth tended to decrease the thresholds and increase the magnitude of both the short- and long-latency neuronal responses and the short-latency digastric response.


2003 ◽  
Vol 90 (2) ◽  
pp. 566-577 ◽  
Author(s):  
Darryl T. Hamamoto ◽  
Donald A. Simone

Acetic acid applied to the hind limb of a frog evokes nocifensive behaviors, including a vigorous wiping of the exposed skin, referred to as the wiping response. The aim of this study was to examine the responses of cutaneous primary afferent fibers in frogs to acetic acid (pH 2.84–1.42) applied topically to the skin. Conventional electrophysiological methods were used to record neuronal activity from single identified primary afferent fibers with cutaneous receptive fields on the hind limb. Fibers were classified according to their conduction velocities and responses evoked by mechanical and thermal (heat and cold) stimuli. One hundred and twenty-two mechanosensitive afferent fibers were studied (44 Aβ, 60 Aδ, and 18 C fibers). Thirty-nine percent of all fibers were excited by acetic acid, but a greater percentage of Aδ (52%) and C fibers (44%) were excited than Aβ fibers (20%). Evoked responses of fibers increased with increasingly more acidic pH until the greatest responses were evoked by acetic acid at pH 2.59–2.41. Application of acetic acid at pHs <2.41 evoked less excitation, suggesting that fibers became desensitized. Similar percentages of nociceptors and low-threshold mechanoreceptors were excited by acetic acid. Thus primary afferent fibers were excited by acetic acid at pHs that have been shown to evoke the wiping response in our previous study. The results of the present study suggest that the model of acetic acid-induced nociception in frogs may be useful for studying the mechanisms by which tissue acidosis produces pain.


1994 ◽  
Vol 72 (2) ◽  
pp. 883-889 ◽  
Author(s):  
D. A. Simone ◽  
P. Marchettini ◽  
G. Caputi ◽  
J. L. Ochoa

1. Intraneural microstimulation (INMS) and microneurography were used in combination to stimulate and record from muscle nociceptor primary afferent fibers of the common peroneal nerve of healthy volunteers. When pain evoked by INMS was projected to muscle, afferent activity could be evoked by innocuous and noxious pressure applied within the projected painful area. Conduction velocity of single fibers was determined by stimulating the receptive fields (RFs) electrically via needle electrodes inserted into the RF and measuring conduction latency and distance between the RF and recording electrode. 2. Pain projected to muscle during INMS trains 5–10 s in duration at threshold intensity for pain sensation was typically described as cramping and was well localized. Subjects mapped the area of the painful projected field (PF) over the skin using a pointer. 3. Fourteen slowly adaping mechanoreceptors with RF in muscle and with moderate to high receptor threshold were identified within or near the painful PF. Conduction velocities were in the range of Group III (n = 8) and Group IV (n = 6) fibers. Mean RF areas of Group III and Group IV afferents, determined by applying pressure percutaneously, were 2.71 +/- 1.14 (SE) cm2 and 3.40 +/- 1.08 (SE) cm2, respectively. Only one Group III afferent unit exhibited spontaneous activity (< 1 Hz). 4. One additional high-threshold mechanoreceptor was identified, with its RF located in the extensor tendon at the base of the big toe. This fiber had a conduction velocity of 32 m/s. During INMS, a well-localized sharp pain was projected to the tendon.(ABSTRACT TRUNCATED AT 250 WORDS)


2017 ◽  
Vol 118 (4) ◽  
pp. 1931-1942 ◽  
Author(s):  
Nicholas D. J. Strzalkowski ◽  
R. Ayesha Ali ◽  
Leah R. Bent

Single unit microneurography was used to record the firing characteristics of the four classes of foot sole cutaneous afferents [fast and slowly adapting type I and II (FAI, FAII, SAI, and SAII)] in response to sinusoidal vibratory stimuli. Frequency (3–250 Hz) and amplitude (0.001–2 mm) combinations were applied to afferent receptive fields through a 6-mm diameter probe. The impulses per cycle, defined as the number of action potentials evoked per vibration sine wave, were measured over 1 s of vibration at each frequency-amplitude combination tested. Afferent entrainment threshold (lowest amplitude at which an afferent could entrain 1:1 to the vibration frequency) and afferent firing threshold (minimum amplitude for which impulses per cycle was greater than zero) were then obtained for each frequency. Increases in vibration frequency are generally associated with decreases in expected impulses per cycle ( P < 0.001), but each foot sole afferent class appears uniquely tuned to vibration stimuli. FAII afferents tended to have the lowest entrainment and firing thresholds ( P < 0.001 for both); however, these afferents seem to be sensitive across frequency. In contrast to FAII afferents, SAI and SAII afferents tended to demonstrate optimal entrainment to frequencies below 20 Hz and FAI afferents faithfully encoded frequencies between 8 and 60 Hz. Contrary to the selective activation of distinct afferent classes in the hand, application of class-specific frequencies in the foot sole is confounded due to the high sensitivity of FAII afferents. These findings may aid in the development of sensorimotor control models or the design of balance enhancement interventions. NEW & NOTEWORTHY Our work provides a mechanistic look at the capacity of foot sole cutaneous afferents to respond to vibration of varying frequency and amplitude. We found that foot sole afferent classes are uniquely tuned to vibration stimuli; however, unlike in the hand, they cannot be independently activated by class-specific frequencies. Viewing the foot sole as a sensory structure, the present findings may aid in the refinement of sensorimotor control models and design of balance enhancement interventions.


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