Parabrachial and hypothalamic interaction in sodium appetite

Abstract

Rats with bilateral lesions of the lateral hypothalamus (LH) fail to exhibit sodium appetite. Lesions of the parabrachial nuclei (PBN) also block salt appetite. The PBN projection to the LH is largely ipsilateral. If these deficits are functionally dependent, damaging the PBN on one side and the LH on the other should also block Na appetite. First, bilateral ibotenic acid lesions of the LH were needed because the electrolytic damage used previously destroyed both cells and axons. The ibotenic LH lesions produced substantial weight loss and eliminated Na appetite. Controls with ipsilateral PBN and LH lesions gained weight and displayed robust sodium appetite. The rats with asymmetric PBN-LH lesions also gained weight, but after sodium depletion consistently failed to increase intake of 0.5 M NaCl. These results dissociate loss of sodium appetite from the classic weight loss after LH damage and prove that Na appetite requires communication between neurons in the LH and the PBN. ibotenic acid; lateral hypothalamus; asymmetric lesions; parabrachial nuclei SALT APPETITE ARISES DURING sodium need or its hormonal mimics. It is usually assessed by measuring NaCl intake at concentrations rejected by animals in hydromineral balance (5,38). Although the hormonal precursors of the Na (sodium) appetite and their neural targets are yielding to investigation, the neural mechanisms that change the hedonic value of the sapid stimulus remain elusive (6, 10). Bilateral lesions centered in the parabrachial nuclei (PBN), the second central gustatory relay in rodents, eliminate the expression of salt appetite (7,8,41,(43)(44)(45). Chronic decerebrate rats that have an intact PBN but no connections between the hind-and forebrain also fail to express Na appetite (12). Thus, the PBN is necessary for the expression of sodium appetite, but is not sufficient unless its axonal connections to the forebrain are intact. In the forebrain, however, neither the thalamic nor the cortical gustatory areas are required for the expression of this behavior (7,8,41,51,55). Based on these observations, it follows that the gustatory neural activity required for salt appetite reaches the forebrain via the PBN projections to the limbic system (29). Nevertheless, the intermediate structures and functional relationships remain to be deciphered.The major terminal areas of the PBN in the limbic system: 1) amygdala, 2) bed nucleus of the stria terminalis, and 3) lateral hypothalamus (LH), each influence Na appetite to one degree or another (9,36,42,56). These same areas also are connected to the PBN reciprocally, to one another (3, 21), and to key components in a proposed reward system: the prefrontal cortex, ventral tegmental area, and nucleus accumbens (22,24,47). This anatomical complexity confounds any simple prediction about the mechanisms through which the hedonic sign of parabrachial gustatory activity is altered by body sodium deficit.The conventional approach to such an embarrassment of riches is to damage each of the forebrain targets in turn. As menti...

Role of the lateral parabrachial nucleus in the control of sodium appetite

“…Neurons in the gustatory PBN are activated by applying 0.3 M NaCl to the anterior tongue indicating that this portion of the PBN receives signals related to salty taste (32,51,103,116). Bilateral lesions in the gustatory PBN abolish sodium appetite (32, 51, 116).…”

“…Another portion of the PBN, often referred to as the gustatory PBN, includes medial portions of the anatomically defined MPBN and LPBN (32,51,103,116). Neurons in the gustatory PBN are activated by applying 0.3 M NaCl to the anterior tongue indicating that this portion of the PBN receives signals related to salty taste (32,51,103,116).…”

Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat

“…The more extensive input to the LHAjd from the lateral PB suggests a more prominent influence of ascending viscerosensory information (Saper, 2002) LHAjd as a likely recipient of humerosensory information from a circumventricular organ that has a central role in autonomic control (Smith and Ferguson, 2010) and drinking behavior (Smith et al, 1995); however, the SFO and lateral PB input to the LHAjd is relatively small in comparison with the more abundant input to the adjacent LHAs, which also has light bidirectional connections with the LHAjd (present data; Hahn and Swanson, 2010). Among their diverse functions the PB (especially the lateral PB) and the SFO have a major role in the control of water and sodium intake (Smith et al, 1995;Fitzsimons, 1998;Geerling and Loewy, 2008), and more recent work indicates that communication between the PB and the LHA is necessary for the expression of sodium appetite in rats (Dayawansa et al, 2011). Given a hypothetical role for the LHAjd in the control of defensive behaviors, input to the LHAjd from the SFO and lateral PB might provide a neuronal pathway for the modulation of an animal's (defensive) behavior in response to changes in its physiological state.…”

Parabrachial-hypothalamic interactions are required for normal conditioned taste aversions

“…Such an interaction has been demonstrated for salt appetite using rats with asymmetric PBN-LH lesions, i.e., unilateral PBN damage on one side of the brain and unilateral LH lesions on the other (2). A separate set of rats with asymmetrical PBN-LH lesions was used for the CTA acquisition and retention experiments summarized here.…”

“…Thus, the other experiments could not have affected the CTA results. Because some of the experiments have been published (2), the description of the surgical procedures that were common to all of the experiments is abbreviated in what follows.…”