Sympathetic nervous control of the cerebral circulation in sleep

Abstract

Summary Cerebral vessels are extensively innervated by sympathetic nerves arising from superior cervical ganglia, and these nerves might play a protective role during the large arterial pressure surges of active sleep (AS). We studied lambs (n = 10) undergoing spontaneous sleep–wake cycles before and after bilateral removal of the superior cervical ganglia (SCGx, n = 5) or sham ganglionectomy (n = 5). Lambs were instrumented to record cerebral blood flow (CBF, flow probe on the superior sagittal sinus), carotid arterial pressure (Pca), intra‐cranial pressure (Pic), cerebral perfusion pressure (Pcp = Pca−Pic) and cerebral vascular resistance (CVR). Prior to SCGx, CBF (mL min−1) was significantly higher in AS than in Quiet Sleep (QS) and Quiet Wakefulness (QW) (17 ± 2, 13 ± 3, and 14 ± 3 respectively, mean ± SD, P < 0.05). Following SCGx, baseline CBF increased by 34, 31, and 29% respectively (P < 0.05). CVR also decreased in all states by ∼25% (P < 0.05). During phasic AS, surges of Pca were associated with transient increases in Pcp, Pic and CBF. Following SCGx, peak CBF and Pic during surges became higher and more prolonged (P < 0.05). Our study is the first to reveal that tonic sympathetic nerve activity (SNA) constricts the cerebral circulation and restrains baseline CBF in sleep. SNA is further incremented during arterial pressure surges of AS, limiting rises in CBF and Pic, possibly by opposing vascular distension as well as by constricting resistance vessels. Thus, SNA may protect cerebral microvessels from excessive distension during AS, when large arterial blood pressure surges are common.

Sympathetic nerve activity in the superior cervical ganglia increases in response to imposed increases in arterial pressure

“…As some anesthetic agents have been shown to suppress autonomic nervous activity (20), tonic SNA may be more pronounced in conscious animals. Supporting this suggestion, SCG ablation increased baseline cerebral blood flow by ϳ1/3 in lambs undergoing spontaneous sleep-wake cycles in the study of Loos et al (27).…”

“…Stimulation of the sympathetic trunk during acute hypertension limits increases in cerebral blood flow (4,6,41). Cervical ganglionectomy has been shown to result in elevated baseline CBF, as well as greater CBF increases associated with natural blood pressure surges (27). Until the present study, no evidence based on direct neural recordings of SNA during potentially damaging elevations in AP was available.…”

“…Cerebral sympathetic activity appears to limit cerebral perfusion during normal sleep, as baseline cerebral blood flow, as well as the blood flow surges occurring during the natural transient blood pressure surges of REM sleep are augmented after cervical (SCG) sympathectomy in sleeping lambs (27).…”

Cerebral vascular regulation and brain injury in preterm infants

“…Extraparenchymal and intraparenchymal blood vessels are richly innervated by autonomic nerves (111) and have been shown to modify autoregulation. For example, the lower limit of CBF autoregulation is shifted toward higher blood pressure in parasympathetically denervated rats (128), and a similar shift is observed after stimulation of the cerebral sympathetic system (142).…”

Correlation between Sleep Duration and Risk of Stroke

“…It has been demonstrated that tonic sympathetic nerve activity constricts the cerebral circulation and restrains baseline CBF in sleep. 12 Cerebral metabolic rate and CBF decrease during stages 3 and 4 NREM sleep, whereas the partial pressure of arterial CO 2 increases because of a reduction in alveolar ventilation. It has been reported that the cerebral circulation during sleep is regulated by metabolic factors depending on the brain activity at a regional level, PO 2 , PCO 2 , pH changes, and autoregulation.…”