From sensory circumventricular organs to cerebral cortex: Neural pathways controlling thirst and hunger

Abstract

Much progress has been made during the past 30 years with respect to elucidating the neural and endocrine pathways by which bodily needs for water and energy are brought to conscious awareness through the generation of thirst and hunger. One way that circulating hormones influence thirst and hunger is by acting on neurones within sensory circumventricular organs (CVOs). This is possible because the subfornical organ and organum vasculosum of the lamina terminalis (OVLT), the sensory CVOs in the forebrain, and the area postrema in the hindbrain lack a normal blood‐brain barrier such that neurones within them are exposed to blood‐borne agents. The neural signals generated by hormonal action in these sensory CVOs are relayed to several sites in the cerebral cortex to stimulate or inhibit thirst or hunger. The subfornical organ and OVLT respond to circulating angiotensin II, relaxin and hypertonicity to drive thirst‐related neural pathways, whereas circulating amylin, leptin and possibly glucagon‐like peptide‐1 act at the area postrema to influence neural pathways inhibiting food intake. As a result of investigations using functional brain imaging techniques, the insula and anterior cingulate cortex, as well as several other cortical sites, have been implicated in the conscious perception of thirst and hunger in humans. Viral tracing techniques show that the anterior cingulate cortex and insula receive neural inputs from thirst‐related neurones in the subfornical organ and OVLT, with hunger‐related neurones in the area postrema having polysynaptic efferent connections to these cortical regions. For thirst, initially, the median preoptic nucleus and, subsequently, the thalamic paraventricular nucleus and lateral hypothalamus have been identified as likely sites of synaptic links in pathways from the subfornical organ and OVLT to the cortex. The challenge remains to identify the links in the neural pathways that relay signals originating in sensory CVOs to cortical sites subserving either thirst or hunger.

Thirst and Drinking Paradigms: Evolution from Single Factor Effects to Brainwide Dynamic Networks

“…[ [89][90][91][92] Two distinct neural populations in the brain trigger or suppress thirst. This suggests an innate brain circuit that initiates and stops animal water-drinking behavior, and likely functions as a center for thirst control in the brains of mammals.…”

“…All of these processes are represented in Tables 2-5. The ability to assess subjective sensations (i.e., using rating scales) during human imaging offers a great advantage over animal experiments, because the intensity of thirst, taste and other sensations can be correlated with changes of regional blood flow in the brain [92].…”

Anterior cingulate cortex modulates the affective‐motivative dimension of hyperosmolality‐induced thirst

“…Many brain regions spanning the cortex, thalamus, midbrain and hindbrain either receive direct axonal projections from the lamina terminalis or functionally relate to thirst (McKinley et al . ). In particular, the medial thalamic anterior cingulate cortex (ACC) system receives thirst‐relevant signals from the subcortical SFO, OVLT and MnPO network (Farrell et al .…”

“…In contrast to these well-established autonomic and neuroendocrine pathways, the neuronal basis for the affective-motivative dimension of drinking behaviour remains poorly defined . Many brain regions spanning the cortex, thalamus, midbrain and hindbrain either receive direct axonal projections from the lamina terminalis or functionally relate to thirst (McKinley et al 2019). In particular, the medial thalamic anterior cingulate cortex (ACC) system receives thirst-relevant signals from the subcortical SFO, OVLT and MnPO network (Farrell et al 2011).…”

Multiple overlapping hypothalamus-brainstem circuits drive rapid threat avoidance

“…Different homeostatic needs are known to engage specific peptide-releasing hypothalamic neurons to drive adaptive responses. For instance, blood or cerebrospinal fluid hyperosmolarity recruits neurons in the paraventricular hypothalamus that release arginine vasopressin or oxytocin, among other transmitters (McCormick & Bradshaw, 2006;Bourque, 2008;Zimmerman et al, 2017;McKinley et al, 2019). Energy imbalance recruits neurons in the paraventricular hypothalamus that release oxytocin, corticotrophin-releasing hormone, or thyrotropin-releasing hormone, as well as neurons in the arcuate hypothalamus that release neuropeptide-Y (Gao & Horvath, 2007;Aponte et al, 2011;Krashes et al, 2011;Hill, 2012;Sternson, 2013).…”