24.1.1 Blood Column Informs Perception of Posture in Humans

Though it is widely acknowledged that visual and vestibular information plays a major role in maintaining orientation in space and locomotor equilibrium, the importance of extravestibular mechanoreceptors has only recently been demonstrated. Studies in patients with disturbed vestibular function (due to disease, trauma, or bilateral surgical removal of vestibular organ) showed that their ability to maintain an upright posture is virtually the same as that of normal controls, even in the absence of visual information [11]. It was traditionally assumed that these patients rely on proprioceptive information from joints, tendons and muscles and skin. Psychophysiological experiments by Mittelstaedt and coworkers on patients with labyrinthine dysfunction demonstrated, however, that somatic gravity information is mediated by the shifting column of blood in the large vessels [12]. This was confirmed by placing subjects on a sled centrifuge, rotating at constant speed, in a darkened room (to eliminate visual cues). Shifts of blood were measured by body pletysmography and controlled with application of lower body positive/negative pressure [13]. The experimental protocol was designed to neutralize the gravitational effects on vestibular organs so that the caudal and cranial shifts of blood were interpreted as a head-up or head-down tilt by the subjects, respectively. The findings suggest that in addition to vision, a separate information system for perception of posture exists in humans. It is mediated by the vertical distribution of “blood column” [14].

24.2.1 Experimental Evidence in Animals

To settle the issue, researchers have compared hemodynamic data from nature’s own models ranging from snakes to giraffes. Lillywhite demonstrated a unique adaptation to gravity in aquatic, terrestrial, and tree-climbing snakes which are known to lack venous valves. The position of the heart in the former is close to the middle of the body, it moves proximally in terrestrial species and is located near the head in arboreal species which spend part of their time in the vertical position [23]. (Fig. 24.6) Baroreceptors and dense adrenergic and peptidergic innervation of the heart and vasculature has been identified in terrestrial snakes, pointing to the importance of autonomic control in hemodynamics. Blood pressures in arboreal snakes are two to three times greater (40–80 mm Hg) than in non-climbing and water species (20–30 mm Hg) [24, 25]. Seymor and Arndt postulate that as snakes populated the gravity-free watery environment, they lost the pressure-regulating mechanisms while the tree climbing species developed them further [16]. Collectively, these observations speak against the siphon effect in snakes [16, 20].

The mode of brain perfusion in an adult giraffe, with its head towering 2 or 3 m above the level of the heart, and a similar distance below the heart when stooping to drink, presents a different challenge to physiology. Despite the mean arterial pressure values being twice the value in humans, it has been claimed that cerebral perfusion in giraffe must be supported by the siphon effect [21, 22, 26]. A reference has already been made to the unique morphology of a giraffe’s heart that can maintain such high arterial pressures in the absence of left ventricular hypertrophy (cf. caption d, Fig 11.12).

Hargens and coworkers measured arterial and jugular vein pressures at different points along the giraffe’s neck in upright, sedated animals. Mean venous pressures were 16 mm Hg at the top and 7 mm Hg at the base of the neck, contrary to what would be expected in a column of blood over the same vertical distance (around 90 cm). These paradoxical values were thought to be caused by venous collapse and segmentation of the blood column. Anatomical dissection of the jugular veins showed greater density of the valves at the top of the neck and only a few at the base, suggesting the brain’s protection against the backflow of blood during grazing and drinking.⁵ While the arterial pressure of 110 mm Hg at the top and 190 mm Hg at the base of the neck supported the difference in hydrostatic height, the venous pressures were reversed from expected. Arterial pressures in the artery of the foot were highly variable during walking with values between 70 and 380 mm Hg. Venous and interstitial pressures ranged between −250 and +240, and −120 and +80 mm Hg, respectively. The authors ruled out the siphon effect [28].

These findings were confirmed in a recent study by Brøndum et al. who measured pressures in the aortic arch, carotid artery, and jugular vein in five anesthetized giraffes [29]. Spinal fluid pressure was determined in two animals at the level of cisterna magna. The animals were suspended in a sling in an upright position with the possibility of lowering the neck down to the level of the heart. The mean aortic pressures in the upright position was 193 ± 11 mm Hg and 118 ± 9 mm Hg in the carotid, a difference of 76 ± 4, consistent with the change in hydrostatic pressure. The jugular venous pressure at the cranial end was −7 ± 2 mm Hg and the central venous pressure 4 ± 2 mm Hg in the upright posture. The lowest recorded pressure at the cranial end of the jugular veins was −21 mm Hg.

On head lowering, the carotid pressure increased to 134 ± 7 mm Hg and the aortic pressure decreased to 131 ± 13 mm Hg. The cranial venous pressure increased to 30 ± 3 mm Hg and the central venous pressure dropped to −1 mm Hg. Carotid and jugular flows remained unchanged between the two positions as did the cross sections of the carotid artery. Jugular venous cross-section area changed from 0.14 cm² in the upright to 3.19 cm² in the head down position. No significant difference was found in the jugular and carotid flow between the two positions; however, the cardiac output decreased by 30% during head lowering. The spinal fluid pressures at the cisterna magna were 2 ± 0 mm Hg in the upright and 8 ± 0 mm Hg in the head down position. The authors concluded that the cerebral blood flow in an upright giraffe, though modified by gravity, is supplied by arterial pressure, without support of the siphon effect. They noted, moreover, that a siphon mechanism in a giraffe with 2 m long neck would have to generate either a negative pressures in excess of 100 mm Hg at the level of the head or a high pressure at the base of the jugular vein at the base of the neck, a value not consistent with experimental findings [29].

Even this brief review of the existing literature (many more references could be cited) shows that views on the effect of gravity on circulation are clearly divided with little prospect of resolution. It is difficult to see how the issue can be settled when physicists are yet to agree on the fundamental theory of the siphon effect. In addition to the conventional siphon theory by which gravity pulls the liquid down the descending pipe and creating suction in the ascending pipe,⁶ it has recently been demonstrated that siphons can operate in vacuum and to heights that exceed the so-called barometric limit of the liquid, i.e., the height when the column of fluid ruptures in the pipe (just short of 7 m for water). CO₂ siphons and siphons with discontinuous flows which incorporate bubbles have also been described. Operation of these siphons clearly cannot be explained on principles based on gravity and atmospheric pressure (cf. Ref. [30] for a balanced discussion and further Refs. on the topic).

Amidst the flurry of conjectures Gisolf may have captured the core of the argument by stating that “In the siphon controversy, the role of the brain has curiously been overlooked” [31]. To obtain a better grasp of the issues involved, let us examine some unique features of the cerebral blood flow in humans.