Paraventricular nucleus bicuculline alters frequency components of sympathetic nerve discharge bursts

2001 ◽  
Vol 281 (3) ◽  
pp. H1233-H1241 ◽  
Author(s):  
Michael J. Kenney ◽  
Mark L. Weiss ◽  
Kaushik P. Patel ◽  
Yan Wang ◽  
Richard J. Fels

Autospectral and coherence analyses were used to determine the effect of paraventricular nucleus (PVN) GABAA receptor antagonism [microinfusion or microinjections of bicuculline methiodide (BMI) 100 pmoles] on sympathetic nerve discharge (SND) frequency components (bursting pattern and relationships between discharges in regionally selective nerves) in α-chloralose-anesthetized rats. SND was recorded from the renal, splenic, and lumbar nerves. The following observations were made. First, PVN BMI microinjections, but not PVN saline or cortical BMI microinjections, transformed the cardiac-related SND bursting pattern in baroreceptor-innervated rats to one characterized by the presence of low-frequency bursts not synchronized to the cardiac cycle or phrenic nerve discharge bursts. Second, SND pattern changes were similar in the renal, splenic, and lumbar nerves, and peak coherence values relating low-frequency bursts in sympathetic nerve pairs (renal-splenic, renal-lumbar, and splenic-lumbar) were significantly increased from preinjection control after PVN BMI microinjection. Third, PVN BMI microinjections significantly increased the coupling between low-frequency SND bursts in baroreceptor-denervated rats. Finally, PVN BMI-induced changes in the SND bursting pattern were not observed after PVN pretreatment with muscimol (GABA agonist, 1 nmole). We conclude that PVN GABAA receptor antagonism profoundly alters the frequency components in sympathetic nerves.

1998 ◽  
Vol 275 (6) ◽  
pp. R1992-R2001 ◽  
Author(s):  
Michael J. Kenney ◽  
Dale E. Claassen ◽  
Michelle R. Bishop ◽  
Richard J. Fels

Frequency-domain analyses were used to determine the effect of heat stress on the relationships between the discharge bursts of sympathetic nerve pairs and sympathetic and phrenic nerve pairs in chloralose-anesthetized rats. Sympathetic nerve discharge (SND) was recorded from the renal, splanchnic, splenic, and lumbar nerves during increases in core body temperature (Tc) from 38 to 41.4 ± 0.3°C. The following observations were made: 1) hyperthermia transformed the cardiac-related bursting pattern of SND to a pattern that contained low-frequency, non-cardiac-related bursts, 2) the pattern transformation was uniform in regionally selective sympathetic nerves, 3) hyperthermia enhanced the frequency-domain coupling between SND and phrenic nerve bursts, and 4) low-frequency SND bursts recorded during hyperthermia contained significantly more activity than cardiac-related bursts. We conclude that acute heat stress profoundly affects the organization of neural circuits responsible for the frequency components in sympathetic nerve activity and that SND pattern transformation provides an important strategy for increasing the level of activity in sympathetic nerves during increased Tc.


2006 ◽  
Vol 291 (3) ◽  
pp. R573-R579 ◽  
Author(s):  
Bryan G. Helwig ◽  
Sujatha Parimi ◽  
Chanran K. Ganta ◽  
Richard Cober ◽  
Richard J. Fels ◽  
...  

Hypothermia produced by acute cooling prominently alters sympathetic nerve outflow. Skin sympathoexcitatory responses to skin cooling are attenuated in aged compared with young subjects, suggesting that advancing age influences sympathetic nerve responsiveness to hypothermia. However, regulation of skin sympathetic nerve discharge (SND) is only one component of the complex sympathetic nerve response profile to hypothermia. Whether aging alters the responsiveness of sympathetic nerves innervating other targets during acute cooling is not known. In the present study, using multifiber recordings of splenic, renal, and adrenal sympathetic nerve activity, we tested the hypothesis that hypothermia-induced changes in visceral SND would be attenuated in middle-aged and aged compared with young Fischer 344 (F344) rats. Colonic temperature (Tc) was progressively reduced from 38°C to 31°C in young (3 to 6 mo), middle-aged (12 mo), and aged (24 mo) baroreceptor-innervated and sinoaortic-denervated (SAD), urethane-chloralose anesthetized, F344 rats. The following observations were made. 1) Progressive hypothermia significantly ( P < 0.05) reduced splenic, renal, and adrenal SND in young baroreceptor-innervated F344 rats. 2) Reductions in splenic, renal, and adrenal SND to progressive hypothermia were less consistently observed and, when observed, were generally attenuated in baroreceptor-innervated middle-aged and aged compared with young F344 rats. 3) Differences in splenic, renal, and adrenal SND responses to reduced Tc were observed in SAD young, middle-aged, and aged F344 rats, suggesting that age-associated attenuations in SND responses to acute cooling are not the result of age-dependent modifications in arterial baroreflex regulation of SND. These findings demonstrate that advancing chronological age alters the regulation of visceral SND responses to progressive hypothermia, modifications that may contribute to the inability of aged individuals to adequately respond to acute bouts of hypothermia.


1999 ◽  
Vol 87 (2) ◽  
pp. 732-742 ◽  
Author(s):  
Michael J. Kenney ◽  
Dale E. Claassen ◽  
Richard J. Fels ◽  
Cristina S. Saindon

Frequency-domain analyses were used to determine the effect of cold stress on the relationships between the discharge bursts of sympathetic nerve pairs, sympathetic and aortic depressor nerve pairs, and sympathetic and phrenic nerve pairs in chloralose-anesthetized, baroreceptor-innervated rats. Sympathetic nerve discharge (SND) was recorded from the renal, lumbar, splanchnic, and adrenal nerves during decreases in core body temperature from 38 to 30°C. The following observations were made. 1) Hypothermia produced nonuniform changes in the level of activity in regionally selective sympathetic nerves. Specifically, cold stress increased lumbar and decreased renal SND but did not significantly change the level of activity in splanchnic and adrenal nerves. 2) The cardiac-related pattern of renal, lumbar, and splanchnic SND bursts was transformed to a low-frequency (0–2 Hz) pattern during cooling, despite the presence of pulse-synchronous activity in arterial baroreceptor afferents. 3) Peak coherence values relating the discharges between sympathetic nerve pairs decreased at the cardiac frequency but were unchanged at low frequencies (0–2 Hz), indicating that the sources of low-frequency SND bursts remain prominently coupled during progressive reductions in core body temperature. 4) Coherence of discharge bursts in phrenic and renal sympathetic nerve pairs in the 0- to 2-Hz frequency band increased during mild hypothermia (36°C) but decreased during deep hypothermia (30°C). We conclude that hypothermia profoundly alters the organization of neural circuits involved in regulation of sympathetic nerve outflow to selected regional circulations.


1994 ◽  
Vol 267 (3) ◽  
pp. R830-R840 ◽  
Author(s):  
M. J. Kenney

Frequency-domain analyses were used to characterize basal sympathetic nerve discharge (SND) and to determine the relationships between the activity recorded simultaneously from sympathetic nerves in chloralose-anesthetized, baroreceptor-innervated rats. Discharges were recorded from the splanchnic, renal, and lumbar nerves. The following observations were made. 1) Approximately 65-75% of total power in SND was contained below 9 Hz in either baroreceptor-innervated rats or baroreceptor-denervated rats. 2) Coherence values relating the activity of two nerves were significantly different from zero within this frequency band. 3) The interval between the discharges of two sympathetic nerves was either frequency dependent or constant within the coherent frequency band. 4) The frequency components of SND and the relationships between the activity in two sympathetic nerves could be altered during periods of acute stress. These results suggest that the system responsible for basal SND in rats is composed of either multiple sympathetic generators or multiple filters arranged in parallel, which are capable of producing different outputs. The dynamic nature of these circuits was revealed by the changes that occurred during periods of acute stress.


2003 ◽  
Vol 284 (5) ◽  
pp. H1710-H1720 ◽  
Author(s):  
Michael J. Kenney ◽  
Mark L. Weiss ◽  
Tammy Mendes ◽  
Yan Wang ◽  
Richard J. Fels

Autospectral and coherence analyses were used to determine the role of and interactions between paraventricular nucleus (PVN) nitric oxide, γ-aminobutyric acid (GABA), and the N-methyl-d-aspartic acid (NMDA)-glutamate receptor in regulation of sympathetic nerve discharge (SND) frequency components in anesthetized rats. Four observations were made. First, PVN microinjection of bicuculline (BIC) (GABAAreceptor antagonist), but not single PVN injections of NMDA (excitatory amino acid) or N G-monomethyl-l-arginine (l-NMMA; a nitric oxide synthase inhibitor), altered SND frequency components. Second, combined PVN microinjections ofl-NMMA and NMDA changed the SND bursting pattern; however, the observed pattern change was different from that produced by PVN BIC and not observed after sinoaortic denervation. Third, PVN microinjection of kynurenic acid prevented and reversed BIC-induced changes in the SND bursting pattern. Finally, vascular resistance (renal and splenic) was significantly increased after PVN BIC microinjection despite the lack of change in the level of renal and splenic SND. These data demonstrate that the PVN contains the neural substrate for altering SND frequency components and suggest complex interactions between specific PVN neurotransmitters and between PVN neurotransmitters and the arterial baroreceptor reflex in SND regulation.


1990 ◽  
Vol 259 (3) ◽  
pp. R549-R560 ◽  
Author(s):  
B. Kocsis ◽  
G. L. Gebber ◽  
S. M. Barman ◽  
M. J. Kenney

The coherence function and phase spectrum were used to study the relationships between the discharges of sets of two postganglionic or preganglionic sympathetic nerves in baroreceptor-denervated cats anesthetized with either 5,5-diallylbarbiturate-urethan or alpha-chloralose. Most of the power in sympathetic nerve discharge was contained between 2 and 6 Hz. The coherence values relating the activity of two nerves were significantly different from zero within this frequency band. The phase spectrum was either linear or complex (i.e., showed changes in slope) within the coherent frequency band. We observed three patterns of relationship. The first pattern was characterized by a constant interval between activity in different sympathetic nerves within the coherent frequency band. The second pattern was characterized by a frequency-dependent interval. The third pattern was characterized by uncoupling of the 2- to 6-Hz rhythms in the discharges of different nerves. Switching between these patterns was observed. We suggest that the three patterns reflect different functional states of the central system responsible for the 2- to 6-Hz rhythm. Two models of this system are entertained. The first model is one of a system of coupled oscillators while filtering circuits that receive common inputs are the elements of the second model.


1996 ◽  
Vol 271 (5) ◽  
pp. R1173-R1185 ◽  
Author(s):  
G. L. Gebber ◽  
S. Zhong ◽  
Y. Paitel

Bispectral analysis was used to demonstrate quadratic nonlinear coupling (i.e., phase locking) of different frequency components in inferior cardiac sympathetic nerve discharge (SND) of urethan-anesthetized rats. The complex patterns of SND analyzed included mixtures of 1) the cardiac-related and 10-Hz rhythms, 2) the 10-Hz rhythm and irregular 2-to 6-Hz oscillations, and 3) the 10-Hz rhythm and a lower frequency non-cardiac-related rhythm near 4 Hz. In some cases, the bicoherence function (normalized bispectrum) showed no phase locking of these frequency components. Cases of nil bicoherence are equated with linear superposition of frequency components, which implies the existence of multiple and noninteractive central circuits. Increased complexity of SND was observed in other cases, as evidenced by significant phase locking of different frequency components with or without frequency locking. Frequency locking (higher frequency rhythm is a multiple of lower) was confirmed by constructing Lissajous orbital plots showing covariation of voltages in selectively filtered bands of SND. We equate frequency locking with nonlinear coupling of the central generators of different sympathetic nerve rhythms and phase locking without frequency locking possibly with nonlinearities arising at levels below noncoupled central rhythm generators.


1981 ◽  
Vol 240 (5) ◽  
pp. R335-R347 ◽  
Author(s):  
S. M. Barman ◽  
G. L. Gebber

The relationships among the spontaneous activity of single neurons in the cat medulla and inferior cardiac sympathetic nerve discharge (SND), electroencephalogram (EEG) activity, phrenic nerve activity, and the R wave of the electrocardiogram were studied with the methods of spike-triggered averaging and postevent interval analysis. Three categories of neurons (SR, SE, and S) with activity patterns related to SND wee identified. The activity of SR units was related in time to SND and the R wave but not to EEG activity. SE unit discharges were related to SND and EEG activity but not to the R wave. S unit activity was related only to SND. Each of the three categories of neurons could be subdivided into two groups depending on whether their discharges were followed by an increase or a decrease in SND. All unit types exhibited respiratory-related discharge patterns. These data are discussed with regard to the problems associated with the identification of neurons in brain stem networks that govern the discharges of sympathetic nerves.


1980 ◽  
Vol 239 (2) ◽  
pp. H143-H155 ◽  
Author(s):  
G. L. Gebber

The current state of knowledge concerning central mechanisms responsible for the generation of background discharges in sympathetic nerves is examined. It is apparent from recent investigations that the classic concept of a randomly discharging and diffusely organized central network onto which rhythms (cardiac- and respiratory-related) are imposed by extrinsic inputs has not passed the test of time. Rather, brain stem as well as spinal networks that govern the discharges of sympathetic nerves are inherently capable of rhythm generation. Sympathetic nerve rhythms inherent to the central nervous system imply the existence of neuronal circuits that are capable of oscillatory activity. Central oscillators provide a mechanism for synchronization of the activity of populations of sympathetic neurons in the absence of periodic input from sources extrinsic to the central nervous system. Indeed, the thesis is developed that, rather than creating rhythms in sympathetic nerve discharge, the function of periodic input from extrinsic sources such as the baroreceptors is to entrain rhythms of central origin. Finally, the problems associated with the identification of neuronal types that comprise central oscillators which govern the discharges of sympathetic nerves are discussed.


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