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

Abstract

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.

Functional and structural changes in the brain associated with the increase in muscle sympathetic nerve activity in obstructive sleep apnoea

“…In experimental animals, 30 days of CIH exposure evokes c-fos expression in the cingulate cortex (Sica et al, 2000b). Consistent with our findings, orthostatic stressors, such as lower-body negative pressure, and inspiratory-capacity apnoea, which unload baroreceptors and increase MSNA, are associated with increased ACC signal activity (Goswami et al, 2012; Macefield et al, 2006), and heart rate variability is associated with changes in activity within both the ACC and retrosplenial cortex (Critchley et al, 2003). The combined evidence demonstrates a key role for the ACC and retrosplenial cortex in the autonomic circuitry, and hence the present findings of altered activity in OSA raise the possibility that dysfunction in these brain regions contributes to the sympathoexcitation in OSA.…”

Cutaneous Mechanoreceptor Feedback from the Hand and Foot Can Modulate Muscle Sympathetic Nerve Activity

“…Goswami and colleagues demonstrated the involvement of the CAN in processing muscle afferent feedback through combined functional magnetic resonance imagining and electrical skin stimulation of forearm muscle afferents (Goswami et al, 2011). Subsequently, electrical stimulation of skeletal muscle afferents was shown to attenuate muscle sympathetic activation by ~4 bursts/minute during baroreceptor unloading using lower body negative pressure without altering heart rate, cardiac output, or mean arterial pressure (Goswami et al, 2012). No changes in MSNA were evident during combined skeletal muscle somatosensory stimulation and an expiratory apnea (Goswami et al, 2012), suggesting that muscle afferents do not converge with chemoreceptor inputs.…”

“…Subsequently, electrical stimulation of skeletal muscle afferents was shown to attenuate muscle sympathetic activation by ~4 bursts/minute during baroreceptor unloading using lower body negative pressure without altering heart rate, cardiac output, or mean arterial pressure (Goswami et al, 2012). No changes in MSNA were evident during combined skeletal muscle somatosensory stimulation and an expiratory apnea (Goswami et al, 2012), suggesting that muscle afferents do not converge with chemoreceptor inputs. Whether cutaneous afferents are associated similarly with the CAN is unclear as this previous work anesthetized the skin to limit their influence (Goswami et al, 2011, 2012).…”

“…However, the interpretation of results is limited by the observation that electrical stimulation can evoke arousal responses that also modulate efferent peripheral sympathetic activity in a similar manner as flashing light (i.e., not dependent on cutaneous mechanoreceptor afferent activity; Donadio et al, 2002a). Cutaneous electrical stimulation can also activate muscle (Goswami et al, 2012) and pain (Nordin and Fagius, 1995) afferents, limiting its use as a tool to understand the selective influence of low threshold mechanoreceptor feedback on cardiovascular control.…”

Coronary artery disease affects cortical circuitry associated with brain-heart integration during volitional exercise

“…An initial important observation of the current study was the difference in HR responses to IHG between the current participants and those of younger individuals reported earlier from our laboratory (Goswami et al 2012;Norton et al 2013;Wong et al 2007). This difference was statistically significant, as determined by an independent group's t-test that contrasted the present data with those published earlier.…”