Integrative Role of the Lamina Terminalis in the Regulation of Cardiovascular and Body Fluid Homeostasis

Abstract

1. Cardiovascular and body fluid homeostasis depends upon the activation and co-ordination of reflexes and behavioural responses. In order to accomplish this, the brain receives and processes both neural and chemical input. Once in the brain, information from sources signalling the status of the cardiovascular system and body fluid balance travels, and is integrated, throughout a widely distributed neural network. Recent studies using neuroanatomical and functional techniques have identified several key areas within this neural network. One major processing node is comprised of structures located along the lamina terminalis. 2. Structures associated with the lamina terminalis include the median preoptic nucleus (MePO) and two sensory circumventricular organs (SCVO), the subfornical organ (SFO) and the organum vasculosum of the lamina terminalis (OVLT). Current evidence indicates that blood-borne signals, such as angiotensin II (AngII), reach SCVO (e.g. SFO) where they are transduced. This information is then carried via neural pathways to brain nuclei (e.g. MePO) where it is integrated with other inputs, such as those derived from systemic arterial blood pressure and volume receptors. 3. Because of their receptive and integrative functions, lamina terminalis structures are essential for the normal control of hormone release (e.g. vasopressin), sympathetic activation and behaviours (thirst and salt appetite), which collectively contribute to maintenance of cardiovascular and body fluid homeostasis.

Vagal afferent input alters the discharge of osmotic and ANG II-responsive median preoptic neurons projecting to the hypothalamic paraventricular nucleus

“…Previous studies strongly indicate that the MnPO plays a pivotal role in autonomic, neuroendocrine, and behavioral responses to body fluid homeostatic challenges (Johnson and Loewy, 1990;Johnson et al, 1996). The present findings along with our previous study (Stocker and Toney, 2005) demonstrate that MnPO-PVH neurons integrate multiple signals including circulating ANG II, osmotic, baroreceptor, and visceral information arising from vagal afferent fibers.…”

“…Anatomical and functional studies suggest the MnPO serves as a forebrain integration site for both humoral and visceral afferent information (Johnson and Loewy, 1990;Johnson et al, 1996). In this regard, our laboratory (Stocker and Toney, 2005) and others (Knuepfer et al, 1985;McAllen et al, 1990;Tanaka et al, 1993;Tanaka et al, 1995;Aradachi et al, 1996) have shown that MnPO neurons are responsive to changes in plasma osmolality, circulating ANG II, and/or changes in ABP.…”

“…The median preoptic (MnPO) nucleus serves as a forebrain integration site for both humoral and visceral signals related to body fluid homeostasis and cardiovascular regulation (Johnson and Loewy, 1990;Johnson et al, 1996). Lesions of the MnPO disrupt the drinking behavior in response to hyperosmolality, ANG II and hypovolemia (Mangiapane et al, 1983;Cunningham et al, 1991;Cunningham et al, 1992), attenuate vasopressin secretion during increase plasma osmolality and ANG II levels (Mangiapane et al, 1983;, and blunt centrally mediated pressor responses to hypertonic saline and ANG II (O'Neill and Brody, 1987;Yasuda et al, 2000).…”

Nitric oxide modulation of the hypothalamo-neurohypophyseal system

“…ANG II produced in response to these physiological conditions activates ANG II receptors in the subfornical organ and organum vasculosum laminae terminalis (41) and thereby promotes release of neurohypophyseal hormones. Similar to these effects observed during hypovolemia, NO also modulates hormone secretion in response to ANG II, such that when administered in conjunction with ANG II, L-NAME enhances oxytocin, but not vasopressin secretion (Figure 2E,F).…”

Osmoregulatory fluid intake but not hypovolemic thirst is intact in mice lacking angiotensin

“…It is thought that the active peptides angiotensin II, III, or IV may have roles within the brain in functions as diverse as the regulation of cardiovascular and fluid homeostasis (2,3,11,19,35,40,41,46), reproduction (15), thermoregulation (28), memory (49), cognition, emotional responses to stress and anxiety, cerebral blood flow regulation, and brain developmental processes (39). However, some studies have questioned whether angiotensin is a neuropeptide because of its very low abundance in brain (23) and have proposed that an alternative endogenous ligand may act on angiotensin receptors in the brain (6).…”