The circle of Willis revisited: Forebrain dehydration sensing facilitated by the anterior communicating artery

Abstract

We hypothesize that threat of dehydration provided selection pressure for the evolutionary emergence and persistence of the anterior communicating artery (ACoA – the inter‐arterial connection that completes the Circle of Willis) in early amniotes. The ACoA is a hemodynamically insignificant artery, but, as we argue in this paper, its privileged position outside the blood‐brain barrier gives it a crucial sensing function for the osmolarity of the blood against the background of the rest of the brain, which efficiently protects itself from dehydration. Till now, the questions of why the ACoA evolved, and what its physiological function is, have remained unsatisfactorily answered. The traditional view—that the ACoA serves as a collateral source of vascularization in case of arterial stenosis—is anthropocentric, and not in accordance with principles of natural selection that apply more generally. Diseases underlying arterial stenosis are associated with aging and the human lifestyle, so this cannot explain why the ACoA formed hundreds of millions of years ago and persisted in amniotes to this day. The peculiar hemodynamic properties of the ACoA could be selected traits that allowed for more efficient forebrain detection of dehydration and complex behavioral responses to water loss, a major advantage in the survival of early amniotes. This hypothesis also explains insufficient hydration often seen in elderly humans.

Neurovascular description in the South American plains vizcacha, Lagostomus maximus (Chinchilloidea, Caviomorpha). A study involving evolutionarily related species of Caviomorpha and Muroidea

“…Taken as a whole, the particularities of the vascular architecture highlighted in the compared species would be considered morphological variations throughout the phylogeny (De Vriese et al, 1984;Gillilan, 1972), rather than evolutionary adaptations per se (Matsuo, 2012). Therefore, the general architecture of vessels would have emerged by convergent evolution at the suborder level (Fenrich et al, 2021;Vrselja et al, 2014).…”

“…The high level of structural conservation of the CoW among species established the classic notion of this structure as a safe brain circulation system capable of ensuring the blood flow to the brain in case of obstruction of the internal carotid artery of one hemisphere through the contralateral blood supply by the rostral communicating artery (Goswami et al, 2020; Snell, 2007). However, its function has recently been reviewed due to the very low frequency of stenosis observed in non‐human species (Fenrich et al, 2021; Vrselja et al, 2014) and the structural vascular studies that focus on variations in CoW among species (Aydin et al, 2008; Fenrich et al, 2021; Kuchinka, 2017; Okuyama et al, 2004; Sasahara et al, 2020). Preliminarily, all these results point to a passive system for dissipating pressure and energy as the main function of the CoW as discussed in Burlakoti et al (2017) and Vrselja et al (2014) rather than a safety system as was established by Thomas Willis, 400 years ago.…”

“…The very high metabolic activity of the brain requires a constant supply of oxygenated blood and glucose to maintain its functional and structural integrity (Karbowski, 2011; Markus, 2004). To cover these requirements, the blood flow is directly sent to the different neural regions through the pair of internal carotid arteries supplying the forebrain and the vertebral arteries mainly supplying the brainstem (Fenrich et al, 2021; Lee, 1995). As part of this blood circulation system, the anastomotic system called Circulus arteriosus cerebri was first described by Dr. Thomas Willis in 1664 (Fenrich et al, 2021; García‐Porrero & Hurlé, 2015; Kenney, 1998; Lee, 1995).…”

“…To cover these requirements, the blood flow is directly sent to the different neural regions through the pair of internal carotid arteries supplying the forebrain and the vertebral arteries mainly supplying the brainstem (Fenrich et al, 2021; Lee, 1995). As part of this blood circulation system, the anastomotic system called Circulus arteriosus cerebri was first described by Dr. Thomas Willis in 1664 (Fenrich et al, 2021; García‐Porrero & Hurlé, 2015; Kenney, 1998; Lee, 1995). This system, the circle of Willis (CoW), is located in the ventral side of the brain surrounding the optic chiasm, the tuber cinereum, and the interpeduncular region (Hur et al, 2016; Malcom & Carpenter, 1994; Schaller, 2007), and works in its classical notion as a safe blood circulation system providing collateral flow between the rostral and caudal arterial systems of the brain, establishing alternative pathways between the left and right cerebral hemispheres, to ensure blood flow to the brain in case of arterial stenosis or occlusion (Goswami et al, 2020).…”

Anatomical variations in the cerebral arterial circle of the Saimaa (Pusa hispida saimensis) and Baltic ringed seals (Pusa hispida botnica)

“…Other than naming the arteries forming the cerebral arterial circle, the authors gave little information on the intracranial vasculature of the Baikal ringed seal (Frąckowiak & Godynicki, 1996), preventing detailed comparisons between ring seal subspecies. The rostral communicating artery was reported to be variably present in Carnivora (ICVGAN 2017; Tanaka et al, 2018) and indicated as being involved in the forebrain dehydration sensing (Fenrich et al, 2021), was not present in any of the Saimaa or Baltic ringed seal specimens. Water balance is not an issue for freshwater seals with easy access to drinking water.…”