Vagal afferent inhibition of primate thoracic spinothalamic neurons

1983 ◽  
Vol 50 (4) ◽  
pp. 926-940 ◽  
Author(s):  
W. S. Ammons ◽  
R. W. Blair ◽  
R. D. Foreman

Spinothalamic (ST) neurons in the C8-T5 segments of the spinal cord were examined for responses to electrical stimulation of the left thoracic vagus nerve (LTV). Seventy-one ST neurons were studied in 39 anesthetized monkeys (Macaca fascicularis). Each neuron could be excited by manipulation of its somatic field and by electrical stimulation of cardiopulmonary sympathetic afferent fibers. LTV stimulation resulted in inhibition of the background activity of 43 (61%) ST neurons. Nine (13%) were excited, 3 (4%) were excited and then inhibited, while 16 (22%) did not respond. There was little difference among these groups in terms of the type of somatic or sympathetic afferent input although inhibited cells tended to be more prevalent in the more superficial laminae. The degree of inhibition resulting from LTV stimulation was related, in a linear fashion, to the magnitude of cell activity before stimulation. LTV inhibition of background activity was similar among wide dynamic range, high threshold, and high-threshold cells with inhibitory hair input. Any apparent differences in LTV inhibitory effects among these groups were accounted for by the differences in ongoing cell activity as predicted by linear regression analysis. LTV stimulation inhibited responses of 32 of 32 ST cells to somatic stimuli. In most cases the stimulus was a noxious pinch; however, LTV stimulation also inhibited responses to innocuous stimuli such as hair movement. Bilateral cervical vagotomy abolished the inhibitory effect of LTV stimulation on background activity (six cells) or responses to somatic stimuli (seven cells). Stimulation of the cardiac branch of the vagus inhibited activity of three cells to a similar degree as LTV stimulation, while stimulation of the vagus below the heart was ineffective in reducing activity of 10 cells. We conclude that LTV stimulation alters activity of ST neurons in the upper thoracic spinal cord. Vagal inhibition of ST cell activity was due to stimulation of cardiopulmonary vagal afferent fibers coursing to the brain stem, which appear to activate descending inhibitory spinal pathways. Vagal afferent activity may participate in processing of somatosensory information as well as information related to cardiac pain.

1992 ◽  
Vol 68 (5) ◽  
pp. 1575-1588 ◽  
Author(s):  
S. F. Hobbs ◽  
M. J. Chandler ◽  
D. C. Bolser ◽  
R. D. Foreman

1. Referred pain of visceral origin has three major characteristics: visceral pain is referred to somatic areas that are innervated from the same spinal segments as the diseased organ; visceral pain is referred to proximal body regions and not to distal body areas; and visceral pain is felt as deep pain and not as cutaneous pain. The neurophysiological basis for these phenomena is poorly understood. The purpose of this study was to examine the organization of viscerosomatic response characteristics of spinothalamic tract (STT) neurons in the rostral spinal cord. Interactions were determined among the following: 1) segmental location, 2) effects of input by cardiopulmonary sympathetic, greater splanchnic, lumbar sympathetic, and urinary bladder afferent fibers, 3) location of excitatory somatic field, e.g., hand, forearm, proximal arm, or chest, 4) magnitude of response to hair, skin, and deep mechanoreceptor afferent input, and 5) regional specificity of thalamic projection sites. 2. A total of 89 STT neurons in segments C3-T6 were characterized for responses to visceral and somatic stimuli. Neurons were activated antidromically from the contralateral ventroposterolateral oralis or caudalis nuclei of the thalamus. Cell responses to visceral and somatic stimuli were not different on the basis of the thalamic site of antidromic activation. Recording sites for 61 neurons were located histologically; 87% of lesion sites were located in laminae IV-VII or X. There was no relationship between response properties of the neurons and spinal laminar location. 3. Different responses to visceral stimuli were observed in three zones of the rostral spinal cord: C3-C6, C7-C8, and T1-T6. In C3-C6, urinary bladder distension (UBD) and electrical stimulation of greater splanchnic and lumbar sympathetic afferent fibers inhibited STT cells. Electrical stimulation of cardiopulmonary sympathetic afferents increased cell activity in C5 and C6 and either excited or inhibited STT cells in C3 and C4. In the cervical enlargement (C7-C8), STT cells generally were either inhibited or showed little response to stimulation of visceral afferent fibers. In T1-T6, input from greater splanchnic and cardiopulmonary sympathetic afferent nerves increased activity of STT cells. Lumbar sympathetic afferent input inhibited cells in T1-T2 and had little effect on cells in T3-T6, whereas UBD decreased cell activity in all segments studied. 4. In general, stimulation of somatic structures increased activity of STT neurons in segments that received primary afferent innervation from the excitatory somatic receptive field or in the segments immediately adjacent to these segments. Only input from the forelimb, especially the hand, markedly excited cells in C7 and C8.+


1986 ◽  
Vol 56 (3) ◽  
pp. 785-796 ◽  
Author(s):  
J. E. Tattersall ◽  
F. Cervero ◽  
B. M. Lumb

Single-unit electrical activity has been recorded from 122 viscerosomatic neurons in the T9 and T11 segments of the cat's spinal cord. These neurons were excited by electrical and/or natural stimulation of visceral and somatic afferent fibers. The majority of viscerosomatic neurons (72%) received somatic nociceptive inputs, either exclusively or together with low-threshold somatic inputs. Many of these neurons were excited most strongly by intense mechanical stimulation of subcutaneous tissues, particularly by pinching or squeezing muscle. Twelve viscerosomatic neurons were excited by distensions of the biliary system at levels of biliary pressure greater than 25 mmHg. These intensities of biliary stimulation evoked transient increases in blood pressure, which suggest that the visceral stimuli were of nociceptive nature. The effects of reversible spinalization by cold block were tested on 98 viscerosomatic neurons. Three subgroups of viscerosomatic neurons were distinguished depending on whether their responses to visceral afferent stimulation were increased, decreased, or unchanged in the spinal state. Forty percent of all neurons tested increased the intensity of their responses to visceral stimulation in the spinal state. In addition, many of these neurons developed or increased their background activity and increased their somatic responses in the spinal state. It is concluded that these neurons were subjected to tonic descending inhibition of both somatic and visceral afferent inputs. More than 40% of the neurons in this group were located in or close to lamina V of the dorsal horn. In 44% of all neurons tested the response to visceral stimulation was reduced or abolished by spinalization. The background activity was not affected in the same manner and sometimes even increased during spinalization. The responses to somatic stimuli were fully tested in 11 neurons of this group and were found to be decreased, but not abolished, in nine neurons, unchanged in one cell, and increased in another one. Many of the neurons in this group were located in the ventral horn (laminae VII and VIII). Sixteen percent of all viscerosomatic neurons tested showed no change in their responses to visceral stimulation during spinalization. It is concluded that the visceral input to viscerosomatic neurons in the lower thoracic spinal cord is under considerable descending control, which includes excitation as well as tonic inhibition of visceral afferent information. This may represent part of the widespread effects of visceral nociceptive stimulation.


2004 ◽  
Vol 287 (6) ◽  
pp. H2728-H2738 ◽  
Author(s):  
Fang Hua ◽  
Theresa Harrison ◽  
Chao Qin ◽  
Angela Reifsteck ◽  
Brian Ricketts ◽  
...  

The purpose of this study was to identify central neuronal sites activated by stimulation of cardiac ischemia-sensitive afferent neurons and determine whether electrical stimulation of left vagal afferent fibers modified the pattern of neuronal activation. Fos-like immunoreactivity (Fos-LI) was used as an index of neuronal activation in selected levels of cervical and thoracic spinal cord and brain stem. Adult Sprague-Dawley rats were anesthetized with urethane and underwent intrapericardial infusion of an “inflammatory exudate solution” (IES) containing algogenic substances that are released during ischemia (10 mM adenosine, bradykinin, prostaglandin E2, and 5-hydroxytryptamine) or occlusion of the left anterior descending coronary artery (CoAO) to activate cardiac ischemia-sensitive (nociceptive) afferent fibers. IES and CoAO increased Fos-LI above resting levels in dorsal horns in laminae I–V at C2 and T4 and in the caudal nucleus tractus solitarius. Dorsal rhizotomy virtually eliminated Fos-LI in the spinal cord as well as the brain stem. Neuromodulation of the ischemic signal by electrical stimulation of the central end of the left thoracic vagus excited neurons at the cervical and brain stem level but inhibited neurons at the thoracic spinal cord during IES or CoAO. These results suggest that stimulation of the left thoracic vagus excites descending inhibitory pathways. Inhibition at the thoracic spinal level that suppresses the ischemic (nociceptive) input signal may occur by a short-loop descending pathway via signals from cervical propriospinal circuits and/or a longer-loop descending pathway via signals from the nucleus tractus solitarius.


1986 ◽  
Vol 56 (5) ◽  
pp. 1411-1423 ◽  
Author(s):  
J. E. Tattersall ◽  
F. Cervero ◽  
B. M. Lumb

Single-unit electrical activity has been recorded from 95 viscerosomatic neurons in the T9 and T11 segments of the cat's spinal cord. These neurons were excited by electrical and/or natural stimulation of visceral and somatic afferent fibers. The excitatory and inhibitory effects on these neurons of volleys in somatic and visceral afferent fibers and of electrical and chemical stimulation of the nucleus raphe magnus (NRM) and adjacent areas of the reticular formation (Ret. F.) have been studied. Electrical stimulation of the splanchnic nerve produced, after the initial excitation of the neurons, a period of inhibition lasting for up to 1 s. This inhibition reduced the responsiveness of the neurons to all inputs, somatic and visceral, and was still present after spinalization of the animals with cold block, which indicates a segmental organization of the inhibition. Electrical stimulation of afferent fibers within the somatic receptive field of the neurons produced, after the initial excitation, a period of inhibition similar to that induced by visceral afferent volleys. During this period of inhibition all inputs to the neurons were reduced. Reversible spinalization of the animals with cold block did not abolish this inhibition. On the basis of the effects of reversible spinalization on the visceral input to viscerosomatic neurons, two types of neurons were distinguished: 1) neurons whose visceral responses increased in the spinal state (neurons under tonic descending inhibition) and 2) neurons whose visceral responses were decreased or abolished in the spinal state (neurons subject to descending excitation). Neurons under tonic descending inhibition were inhibited by electrical stimulation of locations within the NRM and Ret. F. This inhibition lasted for less than 100 ms and could be evoked at intensities of stimulation of 100 microA or less. Neurons under descending excitation were also inhibited by electrical stimulation in the NRM and Ret. F. but, in addition, the inhibition was preceded by an excitation in 75% of these neurons. Chemical stimulation with DL-homocysteic acid (DLH) of locations within the NRM and Ret. F. was used to activate cell bodies, but not axons, located in these brain stem sites. The only effect observed following injections of DLH into the NRM and Ret. F. was inhibition of viscerosomatic neurons including those with descending excitation as well as those with descending inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (5) ◽  
pp. 1950-1961 ◽  
Author(s):  
A. R. Evans ◽  
R. W. Blair

1. Various intensities, frequencies, and pulse widths of electrical stimulation of vagal afferent fibers were used to assess the responses of 87 medullary raphe neurons to vagal afferent fiber input in pentobarbital sodium-anesthetized, barodenervated paralyzed cats. Thirty-seven neurons were antidromically activated from the T2-T3 segments of the thoracic spinal cord, and 40 neurons could not be antidromically activated. Neurons were located in the nucleus raphe magnus (79%) and the nucleus raphe obscurus (15%). The remaining 6% of the neurons were not found; however, their locations were comparable in depth and position on the midline with other neurons in the same animals whose locations were identified. 2. The responses of 60 neurons to electrical stimulation of vagal afferent fibers were classified as excitatory (38%), inhibitory (24%), or mixed, (7%). The mixed responses were characterized by excitation at one frequency or intensity and inhibition at another frequency or intensity. The remaining 27 neurons did not clearly respond. 3. The excitatory responses to electrical stimulation of the cervical vagus nerve were intensity and frequency dependent. Inhibitory responses were frequency dependent at lower frequencies of stimulation and both frequency and intensity dependent at higher frequencies. The mixed responses were frequency dependent. Overall, longer pulse widths produced significantly greater responses than shorter pulse widths. 4. Thirty-three neurons were tested for responses to chemical stimulation of vagal afferents with intra-atrial injections of three doses of veratridine. Twenty-one percent were excited, 55% were inhibited, and 6% had mixed responses. For the mixed responses, excitation occurred at one dose and inhibition at another. The remaining 18% of the neurons were unresponsive to veratridine. The excitatory responses were dose dependent, but the inhibitory responses were not. Three doses of phenybiguanide (PBG) were also used to chemically activate vagal afferents in 27 neurons. Eleven percent were excited, 44% were inhibited, and 4% had mixed responses. The remaining 41% were unresponsive to PBG. The excitatory and inhibitory responses were dose dependent. 5. When comparing responses in projection and nonprojection neurons, inhibition was seen significantly more often in projection neurons and excitation in nonprojection neurons. Sixty-three percent of the neurons inhibited by electrical stimulation were raphespinal neurons, and 78% of the neurons excited by vagal stimulation were nonprojection neurons. Similar observations were made with the responses to chemical activation of the vagus. 6. Neurons with lower spontaneous discharge rates were more often excited by vagal stimulation and neurons with higher rates were more often inhibited.(ABSTRACT TRUNCATED AT 400 WORDS)


1991 ◽  
Vol 69 (7) ◽  
pp. 1035-1045 ◽  
Author(s):  
John Ciriello ◽  
Michael B. Gutman

The functional projections from pressor sites in the subfornical organ (SFO) were identified using the 2-deoxyglucose (2-DG) autoradiographic method in urethane-anesthetized, sinoaortic-denervated rats. Autoradiographs of brain and spinal cord sections taken from rats whose SFO was continuously stimulated electrically for 45 min with stereotaxically placed monopolar electrodes (150 μA, 1.5-ms pulse duration, 15 Hz) following injection of tritiated 2-DG were compared with control rats that received intravenous infusions of pressor doses of phenylephrine to mimic the increase in arterial pressure observed during SFO stimulation. Comparisons were also made to autoradiographs from rats in which the ventral fornical commissure (CFV), just dorsal to the SFO, was electrically stimulated. The pressor responses during either electrical stimulation of the SFO or intravenous infusion of phenylephrine were similar in magnitude. On the other hand, stimulation of the CFV did not elicit a significant pressor response. Electrical stimulation of the SFO increased 2-DG uptake, in comparison to the phenylephrine-infused rats, in the nucleus triangularis, septofimbrial nucleus, lateral septal nucleus, nucleus accumbens, bed nucleus of the stria terminalis, dorsal and ventral nucleus medianus (median preoptic nucleus), paraventricular nucleus of the thalamus, hippocampus, supraoptic nucleus, suprachiasmatic nucleus, paraventricular nucleus of the hypothalamus, and the intermediolateral nucleus of and central autonomic area of the thoracic spinal cord. In contrast, in rats whose CFV was stimulated, these nuclei did not demonstrate changes in 2-DG uptake compared with control animals that received pressor doses of phenylephrine. These data have demonstrated some of the components of the neural circuitry likely involved in mediating the pressor responses to stimulation of the SFO and the corrective responses to activation of the SFO by disturbances to circulatory and fluid balance homeostasis.Key words: cardiovascular reflex pathways, drinking, median preoptic nucleus, osmoreceptors, paraventricular nucleus of the hypothalamus, supraoptic nucleus.


1994 ◽  
Vol 266 (1) ◽  
pp. R257-R267 ◽  
Author(s):  
E. W. Akeyson ◽  
L. P. Schramm

To better understand the spinal transmission of visceral afferent information, we conducted neurophysiological studies of single spinal neurons that receive input from the greater splanchnic nerve (GSN). Extracellular single-neuron recordings were made in the thoracic spinal cord of chloralose-anesthetized, paralyzed, and artificially ventilated rats, some of which had undergone acute spinal transection at C1. Neurons were divided into four classes according to their responses to GSN stimulation: one-burst excitatory, two-burst excitatory, biphasic, and inhibited. We then studied the characteristics of the convergent somatic input to each class of neurons using either natural somatic stimuli or electrical stimulation of the iliohypogastric nerve (IHN). Most splanchnic input was mediated by unmyelinated fibers, whereas somatic input was mediated by both unmyelinated and small myelinated fibers. Most of the neurons exhibited somatic receptive fields, and the majority responded to both innocuous and noxious somatic stimuli. However, a small number could be excited only by GSN stimulation. Although a careful analysis of response characteristics indicated that there was a tendency for neurons to exhibit similar responses to electrical stimulation of the GSN and the IHN, we observed many combinations of somatic and visceral responses. We suggest that visceral afferent activity, in addition to being processed via convergent somatovisceral pathways, may be processed by neurons that convey only visceral information or by neurons in which visceral and somatic information is differentially coded.


Sign in / Sign up

Export Citation Format

Share Document