Forebrain organization representing baroreceptor gating of somatosensory afferents within the cortical autonomic network

2012 ◽  
Vol 108 (2) ◽  
pp. 453-466 ◽  
Author(s):  
Ruma Goswami ◽  
Maria Fernanda Frances ◽  
Craig Douglas Steinback ◽  
J. Kevin Shoemaker

Somatosensory afferents are represented within the cortical autonomic network (CAN). However, the representation of somatosensory afferents, and the consequent cardiovascular effects, may be modified by levels of baroreceptor input. Thus, we examined the cortical regions involved with processing somatosensory inputs during baroreceptor unloading. Neuroimaging sessions (functional magnetic resonance imaging [fMRI]) recorded brain activity during 30 mmHg lower-body negative pressure (LBNP) alone and combined with somatosensory stimulation (LBNP+SS) of the forearm ( n = 14). Somatosensory processing was also assessed during increased sympathetic outflow via end-expiratory apnea. Heart rate (HR), blood pressure (BP), cardiac output (Q), and muscle sympathetic nerve activity (MSNA) were recorded during the same protocols in a separate laboratory session. SS alone had no effect on any cardiovascular or MSNA variable at rest. Measures of HR, BP, and Q during LBNP were not different compared with LBNP+SS. The rise in MSNA burst frequency was attenuated during LBNP+SS versus LBNP alone (8 vs. 12 bursts/min, respectively, P < 0.05). SS did not affect the change in MSNA during apnea. Activations within the insula and dorsal anterior cingulate cortex (ACC) observed during LBNP were not seen during LBNP+SS. Anterior insula and ACC activations occurring during apnea were not modified by SS. Thus, the absence of insular and dorsal ACC activity during LBNP+SS along with an attenuation of MSNA burst frequency suggest sympathoinhibitory effects of sensory stimulation during decreased baroreceptor input by a mechanism that includes conjoint insula-dorsal ACC regulation. These findings reveal that the level of baroreceptor input influences the forebrain organization of somatosensory afferents.

2007 ◽  
Vol 292 (2) ◽  
pp. R715-R722 ◽  
Author(s):  
D. S. Kimmerly ◽  
S. Wong ◽  
R. Menon ◽  
J. K. Shoemaker

Generally, women demonstrate smaller autonomic and cardiovascular reactions to stress, compared with men. The mechanism of this sex-dependent difference is unknown, although reduced baroreflex sensitivity may be involved. Recently, we identified a cortical network associated with autonomic cardiovascular responses to baroreceptor unloading in men. The current investigation examined whether differences in the neural activity patterns within this network were related to sex-related physiological responses to lower body negative pressure (LBNP, 5, 15, and 35 mmHg). Forebrain activity in healthy men and women ( n = 8 each) was measured using functional magnetic resonance imaging with blood oxygen level-dependent (BOLD) contrast. Stroke volume (SV), heart rate (HR), and muscle sympathetic nerve activity (MSNA) were collected on a separate day. Men had larger decreases in SV than women ( P < 0.01) during 35 mmHg LBNP only. At 35 mmHg LBNP, HR increased more in males then females (9 ± 1 beats/min vs. 4 ± 1 beats/min, P < 0.05). Compared with women, increases in total MSNA were similar at 15 mmHg LBNP but greater during 35 mmHg LBNP in men [1,067 ± 123 vs. 658 ± 103 arbitrary units (au), P < 0.05]. BOLD signal changes ( P < 0.005, uncorrected) were identified within discrete forebrain regions associated with these sex-specific HR and MSNA responses. Men had larger increases in BOLD signal within the right insula and dorsal anterior cingulate cortex than women. Furthermore, men demonstrated greater BOLD signal reductions in the right amygdala, left insula, ventral anterior cingulate, and ventral medial prefrontal cortex vs. women. The greater changes in forebrain activity in men vs. women may have contributed to the elevated HR and sympathetic responses observed in men during 35 mmHg LBNP.


2007 ◽  
Vol 293 (1) ◽  
pp. H299-H306 ◽  
Author(s):  
D. S. Kimmerly ◽  
S. W. Wong ◽  
D. Salzer ◽  
R. Menon ◽  
J. K. Shoemaker

The cortical regions representing peripheral autonomic reactions in humans are poorly understood. This study examined whether changes in forebrain activity were associated with the altered physiological responses to lower body negative pressure (LBNP) following a single bout of dynamic exercise (POST-EX). We hypothesized that, compared with the nonexercised condition (NO-EX), POST-EX would elicit greater reductions in stroke volume (SV) and larger increases in heart rate (HR) and muscle sympathetic nerve activity (MSNA) during LBNP (5, 15, and 35 mmHg). Forebrain neural activity ( n = 11) was measured using blood oxygen level-dependent (BOLD) functional magnetic resonance imaging. HR, SV, arterial blood pressure (ABP), and MSNA were collected separately. Compared with NO-EX, baseline ABP was reduced, whereas HR and total vascular conductance (TVC) were elevated in POST-EX ( P < 0.05). In both conditions, 5 mmHg LBNP did not elicit a change (from baseline) in any physiological parameter. Compared with NO-EX, 35 mmHg LBNP-mediated decreases in SV and TVC produced greater increases in HR and MSNA during POST-EX ( P < 0.05). The right posterior insula and dorsal anterior cingulate cortex demonstrated a larger decrease in BOLD at 5 mmHg LBNP but greater BOLD increase at 15 and 35 mmHg LBNP POST-EX vs. NO-EX ( P < 0.005). Conversely, the thalamus and ventral medial prefrontal cortex displayed the opposite BOLD activity pattern (i.e., larger increase at 5 mmHg LBNP but greater decrease at 15 and 35 mmHg LBNP POST-EX vs. NO-EX). Our findings suggest that discrete forebrain regions may be involved with the generation of baroreflex-mediated sympathetic and cardiovascular responses elicited by moderate LBNP.


2010 ◽  
Vol 21 (7) ◽  
pp. 931-937 ◽  
Author(s):  
C. Nathan DeWall ◽  
Geoff MacDonald ◽  
Gregory D. Webster ◽  
Carrie L. Masten ◽  
Roy F. Baumeister ◽  
...  

Pain, whether caused by physical injury or social rejection, is an inevitable part of life. These two types of pain—physical and social—may rely on some of the same behavioral and neural mechanisms that register pain-related affect. To the extent that these pain processes overlap, acetaminophen, a physical pain suppressant that acts through central (rather than peripheral) neural mechanisms, may also reduce behavioral and neural responses to social rejection. In two experiments, participants took acetaminophen or placebo daily for 3 weeks. Doses of acetaminophen reduced reports of social pain on a daily basis (Experiment 1). We used functional magnetic resonance imaging to measure participants’ brain activity (Experiment 2), and found that acetaminophen reduced neural responses to social rejection in brain regions previously associated with distress caused by social pain and the affective component of physical pain (dorsal anterior cingulate cortex, anterior insula). Thus, acetaminophen reduces behavioral and neural responses associated with the pain of social rejection, demonstrating substantial overlap between social and physical pain.


2003 ◽  
Vol 284 (4) ◽  
pp. H1198-H1204 ◽  
Author(s):  
D. S. Kimmerly ◽  
J. K. Shoemaker

We previously demonstrated that diuretic-induced hypovolemia resulted in an enhanced baroreflex-mediated increase in integrated muscle sympathetic nerve activity (MSNA) and vasomotor tone during lower body negative pressure (LBNP) ( Am J Physiol Heart Circ Physiol 282: H645–H655, 2002). The purpose of this study was to perform a retrospective analysis of these data and examine the ability of relative MSNA burst amplitude distributions to highlight differences in baseline sympathetic nerve discharge patterns. An additional purpose was to determine whether differential responses in MSNA burst frequency and burst amplitude affect conclusions regarding sympathetic reflex control. MSNA, stroke volume (SV, Doppler), and estimated central venous pressure (CVP, dependent arm technique) were measured during LBNP within the placebo (Normo) and diuretic (Hypo; 100 mg/day spironolactone for 3 days) conditions ( n = 8). Compared with Normo, MSNA burst frequency at rest was elevated, and there was a rightward shift in the median of the relative burst amplitude distribution ( P < 0.05) in Hypo. During LBNP, the larger rise in total MSNA during Hypo versus Normo was due to greater increases in relative burst amplitude with no difference in the burst frequency response. The MSNA burst frequency response to LBNP was shifted to a higher position on the same MSNA-CVP curve during Hypo compared with Normo. In contrast, the Hypo burst amplitude response was shifted to a new curve with a slope that was similar to the Normo relationship. These data support the use of probability distribution analysis to examine intraindividual differences in baseline and reflex-mediated increases in MSNA burst amplitude. Furthermore, the differential effect of hypovolemia on the responses of burst frequency and amplitude during graded LBNP suggests that burst frequency data alone may not adequately represent reflex control of sympathetic outflow.


2019 ◽  
Vol 117 (2) ◽  
pp. 950-958 ◽  
Author(s):  
Yilu Wang ◽  
Jianqiao Ge ◽  
Hanqi Zhang ◽  
Haixia Wang ◽  
Xiaofei Xie

Engaging in altruistic behaviors is costly, but it contributes to the health and well-being of the performer of such behaviors. The present research offers a take on how this paradox can be understood. Across 2 pilot studies and 3 experiments, we showed a pain-relieving effect of performing altruistic behaviors. Acting altruistically relieved not only acutely induced physical pain among healthy adults but also chronic pain among cancer patients. Using functional MRI, we found that after individuals performed altruistic actions brain activity in the dorsal anterior cingulate cortex and bilateral insula in response to a painful shock was significantly reduced. This reduced pain-induced activation in the right insula was mediated by the neural activity in the ventral medial prefrontal cortex (VMPFC), while the activation of the VMPFC was positively correlated with the performer’s experienced meaningfulness from his or her altruistic behavior. Our findings suggest that incurring personal costs to help others may buffer the performers from unpleasant conditions.


2002 ◽  
Vol 88 (3) ◽  
pp. 1400-1406 ◽  
Author(s):  
Matthew C. Hagen ◽  
David H. Zald ◽  
Tricia A. Thornton ◽  
José V. Pardo

Three inferior prefrontal regions in the monkey receive afferents from somatosensory cortices: the orbitofrontal cortex (OFC), the ventral area of the principal sulcus, and the anterior frontal operculum. To determine whether these areas show responses to tactile stimuli in humans, we examined data from an ongoing series of PET studies of somatosensory processing. Unlike previous work showing ventral frontal activity to hedonic (pleasant/unpleasant) sensory stimulation, the tactile stimuli used in these studies had a neutral hedonic valence. Our data provide evidence for at least two discrete ventral frontal brain regions responsive to somatosensory stimulation: 1) the posterior inferior frontal gyrus (IFG) and adjacent anterior frontal operculum, and 2) the OFC. The former region (posterior IFG/anterior frontal operculum) may have a more specific role in attending to tactile stimuli.


1987 ◽  
Vol 63 (6) ◽  
pp. 2558-2562 ◽  
Author(s):  
R. G. Victor ◽  
W. N. Leimbach

Recent studies indicate that nonhypotensive orthostatic stress in humans causes reflex vasoconstriction in the forearm but not in the calf. We used microelectrode recordings of muscle sympathetic nerve activity (MSNA) from the peroneal nerve in conscious humans to determine if unloading of cardiac baroreceptors during nonhypotensive lower body negative pressure (LBNP) increases sympathetic discharge to the leg muscles. LBNP from -5 to -15 mmHg had no effect on arterial pressure or heart rate but caused graded decreases in central venous pressure and corresponding large increases in peroneal MSNA. Total MSNA (burst frequency X mean burst amplitude) increased by 61 +/- 22% (P less than 0.05 vs. control) during LBNP at only -5 mmHg and rose progressively to a value that was 149 +/- 29% greater than control during LBNP at -15 mmHg (P less than 0.05). The major new conclusion is that nonhypotensive LBNP is a potent stimulus to muscle sympathetic outflow in the leg as well as the arm. During orthostatic stress in humans, the cardiac baroreflex appears to trigger a mass sympathetic discharge to the skeletal muscles in all of the extremities.


2020 ◽  
Author(s):  
Macià Buades-Rotger ◽  
Martin Göttlich ◽  
Ronja Weiblen ◽  
Pauline Petereit ◽  
Thomas Scheidt ◽  
...  

AbstractWinners are commonly assumed to compete more aggressively than losers. Here, we find overwhelming evidence for the opposite. We first demonstrate that low-ranking teams commit more fouls than they receive in top-tier soccer, ice hockey, and basketball leagues. We replicate this effect in the laboratory, showing that participants deliver louder sound blasts to a rival when placed in a low-status position. Using neuroimaging, we characterize brain activity patterns that encode competitive status as well as those that facilitate status-dependent aggression. These analyses reveal three key findings. First, anterior hippocampus and striatum contain multivariate representations of competitive status. Second, interindividual differences in status-dependent aggression are linked with a sharper status differentiation in the striatum and with greater reactivity to status-enhancing victories in the dorsal anterior cingulate cortex. Third, activity in ventromedial, ventrolateral, and dorsolateral prefrontal cortex is associated with trial-wise increases in status-dependent aggressive behavior. Taken together, our results run counter to narratives glorifying aggression in competitive situations. Rather, we show that those in the lower ranks of skill-based hierarchies are more likely to behave aggressively and identify the potential neural basis of this phenomenon.


2018 ◽  
Vol 49 (5) ◽  
pp. 852-860 ◽  
Author(s):  
Jiao Li ◽  
Xujun Duan ◽  
Qian Cui ◽  
Huafu Chen ◽  
Wei Liao

AbstractBackgroundMajor depressive disorder (MDD) is associated with high risk of suicide. Conventional neuroimaging works showed abnormalities of static brain activity and connectivity in MDD with suicidal ideation (SI). However, little is known regarding alterations of brain dynamics. More broadly, it remains unclear whether temporal dynamics of the brain activity could predict the prognosis of SI.MethodsWe included MDD patients (n = 48) with and without SI and age-, gender-, and education-matched healthy controls (n = 30) who underwent resting-state functional magnetic resonance imaging. We first assessed dynamic amplitude of low-frequency fluctuation (dALFF) – a proxy for intrinsic brain activity (iBA) – using sliding-window analysis. Furthermore, the temporal variability (dynamics) of iBA was quantified as the variance of dALFF over time. In addition, the prediction of the severity of SI from temporal variability was conducted using a general linear model.ResultsCompared with MDD without SI, the SI group showed decreased brain dynamics (less temporal variability) in the dorsal anterior cingulate cortex, the left orbital frontal cortex, the left inferior temporal gyrus, and the left hippocampus. Importantly, these temporal variabilities could be used to predict the severity of SI (r = 0.43, p = 0.03), whereas static ALFF could not in the current data set.ConclusionsThese findings suggest that alterations of temporal variability in regions involved in executive and emotional processing are associated with SI in MDD patients. This novel predictive model using the dynamics of iBA could be useful in developing neuromarkers for clinical applications.


2014 ◽  
Vol 45 (3) ◽  
pp. 589-600 ◽  
Author(s):  
J. Gilleen ◽  
S. S. Shergill ◽  
S. Kapur

BackgroundPatients with schizophrenia have substantially reduced subjective well-being (SW) compared to healthy individuals. It has been suggested that diminished SW may be related to deficits in the neural processing of reward but this has not been shown directly. We hypothesized that, in schizophrenia, lower SW would be associated with attenuated reward-related activation in the reward network.MethodTwenty patients with schizophrenia with a range of SW underwent a functional magnetic resonance imaging (fMRI) reward task. The brain activity underlying reward anticipation and outcome in schizophrenia was examined and compared to that of 12 healthy participants using a full factorial analysis. Region of interest (ROI) analyses of areas within the reward network and whole-brain analyses were conducted to reveal neural correlates of SW.ResultsReward-related neural activity in schizophrenia was not significantly different from that of healthy participants; however, the patients with schizophrenia showed significantly diminished SW. Both ROI and whole-brain analyses confirmed that SW scores in the patients correlated significantly with activity, specifically in the dorsal anterior cingulate cortex (dACC), during both reward anticipation and reward outcome. This association was not seen in the healthy participants.ConclusionsIn patients with schizophrenia, reduced activation of the dACC during multiple aspects of reward processing is associated with lower SW. As the dACC has been widely linked to coupling of reward and action, and the link to SW is apparent over anticipation and outcome, these findings suggest that SW deficits in schizophrenia may be attributable to reduced integration of environmental rewarding cues, motivated behaviour and reward outcome.


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