Activity in the Hypothalamus, Amygdala, and Cortex Generates Bilateral and Convergent Modulation of Pontine Gustatory Neurons

2004 ◽  
Vol 91 (3) ◽  
pp. 1143-1157 ◽  
Author(s):  
Robert F. Lundy ◽  
Ralph Norgren

Evidence suggests that centrifugal modulation of brain stem gustatory cells might play a role in the elaboration of complex taste-guided behaviors like conditioned taste aversion and sodium appetite. We previously showed that activity in one forebrain area, the central nucleus of the amygdala (CeA), increased the chemical selectivity of taste cells in the parabrachial nucleus (PBN). The present study investigates how activity in 2 other similarly interconnected forebrain sites, the lateral hypothalamus (LH) and gustatory cortex (GC), might influence PBN gustatory processing in rats. The potential convergence of descending inputs from these sites, as well as the CeA, was also evaluated. After anesthesia (35 mg/kg Nembutal ip), 70 PBN gustatory neurons were tested before, during, and after electrical stimulation of these forebrain sites, while responding to 0.3 M sucrose, 0.1 M NaCl, 0.01 M citric acid, and 0.003 M QHCl. Although each forebrain site modulated taste-evoked responses, more PBN neurons were influenced by stimulation of the GC (67%) and CeA (73%) than of the LH (48%). Activation of cortex (71%) and amygdala (85%) most often produced inhibition, whereas inhibition and excitation occurred equally often during hypothalamic stimulation. Of the neurons tested for convergence ( n = 60), 88% were influenced by ≥1 of the 3 sites. Twenty were modulated by stimulation at all 3 sites and another 17 by 2 of the 3 sites. The net effect of centrifugal modulation was to sharpen the across-stimulus response profiles of PBN cells, particular with regard to the NaCl- and citric acid-best cells.

2005 ◽  
Vol 93 (3) ◽  
pp. 1183-1196 ◽  
Author(s):  
Cheng-Shu Li ◽  
Young K. Cho ◽  
David V. Smith

The lateral hypothalamus (LH) and the central nucleus of the amygdala (CeA) exert an influence on ingestive behavior and are reciprocally connected to gustatory and viscerosensory areas, including the nucleus of the solitary tract (NST) and the parabrachial nuclei (PbN). We investigated the effects of LH and CeA stimulation on the activity of 101 taste-responsive neurons in the hamster PbN. Eighty three of these neurons were antidromically activated by stimulation of these sites; 57 were antidromically driven by both. Of these 83 neurons, 21 were also orthodromically activated—8 by the CeA and 3 by the LH. Additional neurons were excited ( n = 5) or inhibited ( n = 8) by these forebrain nuclei but not antidromically activated. Taste stimuli were: 0.032 M sucrose, 0.032 M sodium chloride (NaCl), 0.032 M quinine hydrochloride (QHCl), and 0.0032 M citric acid. Among the 34 orthodromically activated neurons, more sucrose-best neurons were excited than inhibited, whereas the opposite occurred for citric-acid- and QHCl-best cells. Neurons inhibited by the forebrain responded significantly more strongly to citric acid and QHCl than cells excited by these sites. The effects of electrical stimulation were mimicked by microinjection of dl-homocysteic acid, indicating that cells at these forebrain sites were responsible for these effects. These data demonstrate that many individual PbN gustatory neurons project to both the LH and CeA and that these areas modulate the gustatory activity of a subset of PbN neurons. This neural substrate is likely involved in the modulation of taste activity by physiological and experiential factors.


1995 ◽  
Vol 269 (3) ◽  
pp. R647-R661 ◽  
Author(s):  
K. Nakamura ◽  
R. Norgren

The activity of single taste neurons was recorded from the nucleus of the solitary tract before (n = 41) and after (n = 58) awake, behaving rats were switched to a sodium-free diet. During sodium deprivation, the spontaneous activity of the neurons increased (142%), but responses to water and sapid stimuli decreased. For all neurons in the sample, the mean response to water decreased to 72% of its predeprivation level, NaCl dropped to 53%, sucrose to 41%, citric acid to 68%, and quinine HCl to 84%. Despite the drop in magnitude, the response profiles of the taste neurons were not changed by the dietary condition. In the Na-replete state, 61% of the activity elicited by NaCl occurred in NaCl-best cells and 33% in sucrose-best neurons. In the depleted state, these values were 60 and 26%, respectively. Nevertheless, at the highest concentrations tested, deprivation did alter the relative responsiveness of the gustatory neurons to sucrose and NaCl in specific categories of neurons. Compared with acute preparations, dietary sodium deprivation in awake, behaving rats produced a more general reduction in the gustatory responses of neurons in the nucleus of the solitary tract. The largest reductions in elicited activity occurred for the "best stimulus" of a particular neuron, thus leading to smaller differences in response magnitude across stimuli, particularly at the highest concentrations tested.


1997 ◽  
Vol 78 (2) ◽  
pp. 920-938 ◽  
Author(s):  
Christopher B. Halsell ◽  
Susan P. Travers

Halsell, Christopher B. and Susan P. Travers. Anterior and posterior oral cavity responsive neurons are differentially distributed among parabrachial subnuclei in rat. J. Neurophysiol. 78: 920–938, 1997. The responses of single parabrachial nucleus (PBN) neurons were recorded extracellularly to characterize their sensitivity to stimulation of individual gustatory receptor subpopulations (G neurons, n = 75) or mechanical stimulation of defined oral regions (M neurons, n = 54) then localized to morphologically defined PBN subdivisions. Convergence from separate oral regions onto single neurons occurred frequently for both G and M neurons, but converging influences were more potent when they arose from nearby locations confined to the anterior (AO) or posterior oral cavity (PO). A greater number of G neurons responded optimally to stimulation of AO than to PO receptor subpopulations, and these AO-best G neurons had higher spontaneous and evoked response rates but were less likely to receive convergent input than PO-best G neurons. In contrast, proportions, response rates, and convergence patterns of AO- and PO-best M neurons were more comparable. The differential sensitivity of taste receptor subpopulations was reflected in PBN responses. AO stimulation with NaCl elicited larger responses than PO stimulation; the converse was true for QHCl stimulation. Within the AO, NaCl elicited a larger response when applied to the anterior tongue than to the nasoincisor duct. Hierarchical cluster analysis of chemosensitive response profiles suggested two groups of PBN G neurons. One group was composed of neurons optimally responsive to NaCl (N cluster); the other to HCl (H cluster). Most N- and H-cluster neurons were AO-best. Although they were more heterogenous, all but one of the remaining G neurons were unique in responding best or second-best to quinine and so were designated as quinine sensitive (Q+). Twice as many Q+ neurons were PO- compared with AO-best. M neurons were scattered across PBN subdivisions, but G neurons were concentrated in two pairs of subdivisions. The central medial and ventral lateral subdivisions contained both G and M neurons but were dominated by AO-best N-cluster G neurons. The distribution of G neurons in these subdivisions appeared similar to distributions in most previous studies of PBN gustatory neurons. In contrast to earlier studies, however, the external medial and external lateral-inner subdivisions also contained G neurons, intermingled with a comparable population of M neurons. Unlike cells in the central medial and ventral lateral subnuclei, nearly every neuron in the external subnuclei was PO best, and only one was an N-cluster cell. In conclusion, the present study supports a functional distinction between sensory input from the AO and PO at the pontine level, which may represent an organizing principle throughout the gustatory neuraxis. Furthermore, two morphologically distinct pontine regions containing orosensory neurons are described.


2010 ◽  
Vol 104 (2) ◽  
pp. 726-741 ◽  
Author(s):  
Yi Kang ◽  
Robert F. Lundy

Previous studies have shown that corticofugal input to the first central synapse of the ascending gustatory system, the nucleus of the solitary tract (NST), can alter the way taste information is processed. Activity in other forebrain structures, such as the central nucleus of the amygdala (CeA), similarly influence activation of NST taste cells, although the effects of amygdalofugal input on neural coding of taste information is not well understood. The present study examined responses of 110 NST neurons to 15 taste stimuli before, during, and after electrical stimulation of the CeA in rats. The taste stimuli consisted of different concentrations of NaCl (0.03, 0.1, 0.3 M), sucrose (0.1, 0.3, 1.0 M), citric acid (0.005, 0.01 M), quinine HCl (0.003, 0.03 M), and 0.03 M MSG, 0.1 M KCl, as well as 0.1 M NaCl, 0.01 M citric acid, and 0.03 M MSG mixed with 10 μM amiloride. In 66% of NST cells sampled (73/110) response rates to the majority of effective taste stimuli were either inhibited or augmented. Nevertheless, the magnitude of effect across stimuli was often differential, which provides a neurophysiological mechanism to alter neural coding. Subsequent analysis of across-unit patterns showed that amygdalofugal input plays a role in shaping spatial patterns of activation and could potentially influence the perceptual similarity and/or discrimination of gustatory stimuli by altering this feature of neural coding.


2001 ◽  
Vol 85 (2) ◽  
pp. 770-783 ◽  
Author(s):  
Robert F. Lundy ◽  
Ralph Norgren

Visceral signals and experience modulate the responses of brain stem neurons to gustatory stimuli. Both behavioral and anatomical evidence suggests that this modulation may involve descending input from the forebrain. The present study investigates the centrifugal control of gustatory neural activity in the parabrachial nucleus (PBN). Extracellular responses were recorded from 51 single PBN neurons during application of sucrose, NaCl, NaCl mixed with amiloride, citric acid, and QHCl with or without concurrent electrical stimulation in the ipsilateral central nucleus of the amygdala (CeA). Based on the sapid stimulus that evoked the greatest discharge, 3 neurons were classified as sucrose-best, 32 as NaCl-best, and 16 as citric acid-best. In most of the neurons sampled, response rates to an effective stimulus were either inhibited or unchanged during electrical stimulation of the CeA. Stimulation in the CeA was without effect in two sucrose-best neurons, nine NaCl-best neurons, and one citric acid-best neuron. Suppression was evident in 1 sucrose-best neuron, 18 NaCl-best neurons, and 15 citric acid-best neurons. In NaCl-best neurons inhibited by CeA stimulation, the magnitude of the effect was similar for spontaneous activity and responses to the five taste stimuli. Nonetheless, the inhibitory modulation of gustatory sensitivity increased the relative effectiveness of NaCl resulting in narrower chemical selectivity. For citric acid–best neurons, the magnitude of inhibition produced by CeA activation increased with an increase in stimulus effectiveness. The responses to citric acid were inhibited significantly more than the responses to all other stimuli with the exception of NaCl mixed with amiloride. The overall effect was to change these CA-best neurons to CA/NaCl-best neurons. In a smaller subset of NaCl-best neurons ( n = 5), CeA stimulation augmented the responsiveness to NaCl but was without effect on the other stimuli or on baseline activity. It appears that electrical stimulation in the CeA modulates response intensity, as well as the type of gustatory information that is transmitted in a subset of NaCl-best neurons. These findings provide an additional link between the amygdala and the PBN in the control of NaCl intake, modulating the response and the chemical selectivity of an amiloride-sensitive Na+-detecting input pathway.


2002 ◽  
Vol 87 (1) ◽  
pp. 103-112 ◽  
Author(s):  
Volker Neugebauer ◽  
Weidong Li

Pain has a strong emotional dimension, and the amygdala plays a key role in emotionality. The processing of nociceptive mechanical and thermal information was studied in individual neurons of the central nucleus of the amygdala, the target of the spino-parabrachio-amygdaloid pain pathway and a major output nucleus of the amygdala. This study is the first to characterize nociceptive amygdala neurons with input from deep tissue, particularly the knee joint. In 46 anesthetized rats, extracellular single-unit recordings were made from 119 central amygdala neurons that were activated orthodromically by electrical stimulation in the lateral pontine parabrachial area and were tested for receptive fields in the knee joints. Responses to brief mechanical stimulation of joints, muscles, and skin and to cutaneous thermal stimuli were recorded. Receptive-field sizes and thresholds were mapped and stimulus-response functions constructed. Neurons in the central nucleus of the amygdala with excitatory input from the knee joint ( n = 62) typically had large symmetrical receptive fields in both hindlimbs or in all four extremities and responded exclusively or preferentially to noxious mechanical stimulation of deep tissue ( n = 58). Noxious mechanical stimulation of the skin excited 30 of these neurons; noxious heat activated 21 neurons. Stimulus-response data were best fitted by a sigmoid nonlinear regression model rather than by a monotonically increasing linear function. Another 15 neurons were inhibited by noxious mechanical stimulation of the knee joint and other deep tissue. Fifteen neurons had no receptive field in the knee but responded to noxious stimulation of other body areas; 27 nonresponsive neurons were not activated by natural somesthetic stimulation. Our data suggest that excitation is the predominant effect of brief painful stimulation of somatic tissue on the population of central amygdala neurons with knee joint input. Their large symmetrical receptive fields and sigmoid rather than monotonically increasing linear stimulus-response functions suggest a role of nociceptive central amygdala neurons in other than sensory-discriminative aspects of pain.


2018 ◽  
Author(s):  
María Luisa Torruella-Suárez ◽  
Jessica R. Vandenberg ◽  
Elizabeth S. Cogan ◽  
Gregory J. Tipton ◽  
Adonay Teklezghi ◽  
...  

AbstractThe central nucleus of the amygdala plays a significant role in alcohol use and other affective disorders; however, the genetically-defined neuronal subtypes and their projections that govern these behaviors are not well known. Here we show that neurotensin neurons in the central nucleus of the amygdala of male mice are activated by in vivo ethanol consumption and that genetic ablation of these neurons decreases ethanol consumption and preference in non-ethanol dependent animals. This ablation did not impact preference for sucrose, saccharin, or quinine. We found that the most robust projection of the central amygdala neurotensin neurons was to the parabrachial nucleus, a brain region known to be important in feeding behaviors, conditioned taste aversion, and alarm. Optogenetic stimulation of projections from these neurons to the parabrachial nucleus is reinforcing, and increases ethanol drinking as well as consumption of sucrose and saccharin solutions. These data suggest that this central amygdala to parabrachial nucleus projection influences the expression of reward-related phenotypes and is a novel circuit promoting consumption of ethanol and palatable fluids.


2008 ◽  
Vol 295 (3) ◽  
pp. R751-R763 ◽  
Author(s):  
Suriyaphun S. Mungarndee ◽  
Robert F. Lundy ◽  
Ralph Norgren

For humans and rodents, ingesting sucrose is rewarding. This experiment tested the prediction that the neural activity produced by sapid sucrose reaches reward systems via projections from the pons through the limbic system. Gastric cannulas drained ingested fluid before absorption. For 10 days, the rats alternated an hour of this sham ingestion between sucrose and water. On the final test day, half of them sham drank water and the other half 0.6 M sucrose. Thirty minutes later, the rats were killed and their brains immunohistochemically stained for Fos. The groups consisted of controls and rats with excitotoxic lesions in the gustatory thalamus (TTA), the medial (gustatory) parabrachial nucleus (PBN), or the lateral (visceral afferent) parabrachial nucleus. In controls, compared with water, sham ingesting sucrose produced significantly more Fos-positive neurons in the nucleus of the solitary tract, PBN, TTA, and gustatory cortex (GC). In the ventral forebrain, sucrose sham licking increased Fos in the bed nucleus of the stria terminalis, central nucleus of amygdala, and the shell of nucleus accumbens. Thalamic lesions blocked the sucrose effect in GC but not in the ventral forebrain. After lateral PBN lesions, the Fos distributions produced by distilled H2O or sucrose intake did not differ from controls. Bilateral medial PBN damage, however, eliminated the sucrose-induced Fos increase not only in the TTA and GC but also in the ventral forebrain. Thus ventral forebrain areas associated with affective responses appear to be activated directly by PBN gustatory neurons rather than via the thalamocortical taste system.


2009 ◽  
Vol 101 (3) ◽  
pp. 1598-1612 ◽  
Author(s):  
Laura C. Geran ◽  
Susan P. Travers

Bitterness is a distinctive taste sensation, but central coding for this quality remains enigmatic. Although some receptor cells and peripheral fibers are selectively responsive to bitter ligands, central bitter responses are most typical in broadly tuned neurons. Recently we reported more specifically tuned bitter-best cells (B-best) in the nucleus of the solitary tract (NST). Most had glossopharyngeal receptive fields and few projected to the parabrachial nucleus (PBN), suggesting a role in reflexes. To determine their potential contribution to other functions, the present study investigated whether B-best neurons occur further centrally. Responses from 90 PBN neurons were recorded from anesthetized rats. Stimulation with four bitter tastants (quinine, denatonium, propylthiouracil, cycloheximide) and sweet, umami, salty, and sour ligands revealed a substantial proportion of B-best cells (22%). Receptive fields for B-best NST neurons were overwhelmingly foliate in origin, but in PBN, about half received foliate and nasoincisor duct input. Despite convergence, most B-best PBN neurons were as selectively tuned as their medullary counterparts and response profiles were reliable. Regardless of intensity, cycloheximide did not activate broadly tuned acid/sodium (AN) neurons but did elicit robust responses in B-best cells. However, stronger quinine activated AN neurons and concentrated electrolytes stimulated B-best cells, suggesting that B-best neurons might contribute to higher-order functions such as taste quality coding but work in conjunction with other cell types to unambiguously signal bitter-tasting ligands. In this ensemble, B-best neurons would help discriminate sour from bitter stimuli, whereas AN neurons might be more important in differentiating ionic from nonionic bitter stimuli.


1962 ◽  
Vol 39 (1) ◽  
pp. 13-21 ◽  
Author(s):  
Roger A. Gorski ◽  
Charles A. Barraclough

ABSTRACT We have previously suggested that the failure of the androgen-sterilized, persistent-oestrous rat to ovulate, following electrical stimulation of the median eminence structures of the hypothalamus, is due to an insufficiency in adenohypophyseal LH concentration. Using the ovarian ascorbic acid technique for quantitative determination of pituitary LH content, the present studies have demonstrated that the sterile rat pituitary gland contains one-third the LH content of the normal prooestrous gland. Furthermore, not only does progesterone priming of this persistent-oestrous rat result in a 75 % increase in LH concentration, but on hypothalamic stimulation sufficient LH is released to induce ovulation. The decrease in LH concentration which accompanies ovulation in the progesterone-primed, sterile rat is approximately 45 % of the total gland content as compared with a 51 % decrease in pituitary content in the normal cyclic rat.


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