scholarly journals Response Properties of Whisker-Associated Trigeminothalamic Neurons in Rat Nucleus Principalis

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 (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.


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.


2011 ◽  
Vol 4 (2) ◽  
pp. 343-365 ◽  
Author(s):  
Eiichi Kumamoto ◽  
Kotaro Mizuta ◽  
Tsugumi Fujita

2001 ◽  
Vol 21 (23) ◽  
pp. 9367-9376 ◽  
Author(s):  
David M. Cain ◽  
Paul W. Wacnik ◽  
Michelle Turner ◽  
Gwen Wendelschafer-Crabb ◽  
William R. Kennedy ◽  
...  

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.


Author(s):  
Srinivasa N. Raja ◽  
Richard A. Meyer ◽  
James N. Campbell

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