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© 2005 The American Society for Nutritional Sciences J. Nutr. 135:1486-1490, June 2005

Nutritional Neurosciences

Fos-Positive Neurons Are Increased in the Nucleus of the Solitary Tract and Decreased in the Ventromedial Hypothalamus and Amygdala by a High-Protein Diet in Rats

Nicolas Darcel, Gilles Fromentin, Helen E. Raybould*, Sylvette Gougis, Dorothy W. Gietzen* and Daniel Tomé1

UMR INRA 914 Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris-Grignon, F75231 PARIS Cedex 05, France and * Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616

1To whom correspondence should be addressed. E-mail: tome{at}inapg.fr.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Transition from a normal- (NP) to a high-protein (HP) diet induces a rapid depression in food intake and a progressive but incomplete return to the initial intake during the succeeding days. The aim of this study was to determine which CNS regions are involved in the HP diet–induced satiety in rats. Brains were collected from 3 groups of adult rats after habituation to an NP diet (21 d), during the transition phase to a HP diet (2 d), or after habituation to the HP diet (21 d). Fos expression was measured in several brain areas that are involved in the control of food intake (solitary tract nucleus, anterior piriform cortex, lateral hypothalamus, arcuate nucleus, posterior para ventricular nucleus, medio ventral hypothalamus, dorso medial hypothalamus, amygdala, and accumbens nucleus). Changes occurred in the majority of these regions during the transition period from the NP diet to the HP diet. After habituation to the HP diet, significant changes in Fos expression were restricted to an increase in the nucleus of the solitary tract and a decrease in the ventromedial hypothalamus and the cortex of the amygdala. Considering the functional characteristics of these areas, the present results suggest that the vagus nerve conveys the information relative to the quantity of protein ingested, that hypothalamic sites regulate food intake and may alter sympathetic nervous system activity, and that higher brain functions such as memory processing by the limbic system or food reward system are involved in the HP diet–induced satiety in rats.

KEY WORDS: • brain • vagus nerve • satiety • protein

Protein is considered to be a strong inhibitor of food intake in omnivores and to have the greatest appetite-suppressive effects of the 3 macronutrients (1,2). For instance, increasing the level of dietary protein from 14 to 50% was shown to decrease food intake in freely fed rats, and this effect seemed to be due to an enhancement of satiety rather than to low palatability or to the induction of a conditioned food aversion (3–5). Dietary proteins are also thought to be closely monitored by the central nervous system (CNS),2 especially by central structures such as the hypothalamus and the anterior piriform cortex (APC), regions that control or influence food intake (6,7). Because proteins are likely to be monitored in the same regions in which satiety is thought to originate, dietary proteins may influence the onset of satiety in those regions (8). HP diet–induced satiety may thus provide a promising model for studying satiety in omnivores.

Hypothesizing that dietary protein intake is centrally monitored and may influence central satiety pathways, the specific aims of the present study were to identify the CNS areas involved in the processing of information related to high dietary protein levels. For this purpose, the c-fos immediate early gene product, the Fos protein, was used as a probe for meal-induced neuronal activation in CNS regions involved in the control of food intake, viscerosensitivity, regulation of energy homeostasis, food reward system, and sensation reinforcement (9–13). These include the dorsal motor complex, the hypothalamus, the APC, the accumbens nucleus (ACC), and the extended amygdala.


   MATERIALS AND METHODS
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 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Drugs and chemicals. Pentobarbital sodium was purchased from Sanofi. Primary polyclonal antibody pAb5 raised against Fos protein was purchased from Oncogene Science. Secondary antibody and ABC kits (Vectastain) were purchased from Vector Laboratories. Basic laboratory chemical supplies were purchased from Sigma. Total milk protein was purchased from Armor Protéines; sucrose was purchased from Eurosucre; cornstarch was purchased from Cerestar; vitamin and salt mixtures AIN-93M and choline chloride were purchased from ICN Biomedicals; soy oil was purchased from Bailly; and cellulose was purchased from Medias Filtrants Durieux. Diets were prepared by the Atelier de Préparation des Aliments Expérimentaux (INRA) (Table 1).


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  		TABLE 1 Diet composition (powdered diets)

 
    Animals and feeding schedule. Male Wistar rats (n = 18; Harlan) weighing 200–220 g at the beginning of the experiment were housed individually in hanging wire cages in an artificially illuminated room at 22°C with light onset at 2000 h and a 12-h light:dark cycle; rats had free access to water. Rats were fed a normal-protein (NP) diet for 4 d, then divided into 3 groups of 6 rats, fed for 21 d as follows: the NP-d21 group (habituation to NP) was fed the NP liquid diet for 21 d; the high-protein (HP)-d2 group (transition to HP) was subsequently fed the NP diet and the HP liquid diet for 19 and 2 d, respectively; the HP-d21 group (habituation to HP) was fed the HP liquid diet for 21 d. The daily feeding schedule was as follows: 1) at the end of the light cycle (0800) rats were given a preweighed 2-g calibrated sample of their diet, which they were trained to ingest in 15 min; 2) from 0930 to 1700 h, rats consumed the diet ad libitum. To minimize spillage, both NP and HP diets were moistened (powder:water ratios were 1:1 and 1:2, respectively). Food intake was determined by the difference in weight of the food cup before and after each experimental period, corrected for spillage and evaporation. In the case of the preweighed NP and HP samples, the powder:water ratio was set to 1:1.5 (2 g powder:3 g water). The preweighed meal size was chosen so that the meal could be ingested within 15 min. This procedure allowed comparable experimental volume, weight, and energy meal-induced stimuli regardless of the diet rats were fed on the day of brain collection. Body weights and food intake were monitored daily.

    Tissue collection and immunohistochemical staining. Considering the dynamics of Fos protein expression in the CNS (14), tissue was taken and fixed 90 min after the initial stimulation. On the experimental d 21, rats were fed the preweighed 2-g calibrated sample of their current diet and were killed 90 min later (without consuming their regular ration) with a lethal injection of pentobarbital sodium (90 mg/kg, i.p.). The thoracic cage was opened and rats were perfused intracardially with 500 mL of saline at 37°C followed by 1000 mL of 4% paraformaldehyde in PBS. The forebrain and spinal cord were exposed from the cervical spinal segment C2 to the olfactory bulb; the entire forebrain, cerebellum, and the first 2 cervical spinal segments were removed. This portion of the CNS was cryoprotected using 15% sucrose in PBS for 2 h and then stored in 30% sucrose in PBS with sodium azide to prevent bacterial contamination. The brain regions of interest were localized using a stereotaxic atlas. Transverse 40-µm thick sections corresponding to the regions of interest were cut with a cryostat at –22°C and collected in PBS. One slice in 5 was collected to be processed as a free-floating section and was immunostained for Fos protein according to the avidin-biotin peroxidase method. Sections were incubated in normal goat serum (2% in PBS and 0.3% Triton X-100) for 1 h, then incubated in the primary antiserum containing the polyclonal pAb5 antibody raised against Fos protein diluted 1:5000 for 48 h. Sections were then washed in PBS, incubated in biotinylated goat anti-rabbit antiserum for 24 h, washed, and incubated for 1 h in avidin-peroxidase complex. Staining was developed in 0.05% diaminobenzidine (DAB) with 0.03% hydrogen peroxide. The DAB reaction was halted with several PBS washes, and the sections were mounted on gelatin-coated slides. After being dried overnight, sections were cleared in an ascending series of ethanol baths (70, 95, and 100%, 10 min each bath) followed by a 5-min bath in xylene. Sections were mounted on gelatin-coated slides and cover-slipped. To control for staining variability between days, each immunohistochemistry run contained matched sections from all experimental groups.

    Immunolabeling quantification. Sections were examined with a light microscope; for each rat and each brain region, 5 corresponding sections were chosen for further cell count, and sections were carefully selected to study a constant location in the brain. Analyzed sections were magnified under an Olympus BH-2 light microscope and the image was relayed to a computer through a video camera. Image processing was performed using the video-based analysis system BIO-COM. Pictures were then analyzed using an imaging software; c-fos–positive cells appeared in brown whereas the background remained slightly yellow. Immunolabeling quantification was processed automatically by the imaging program by setting minimum and maximum optical density levels and then manually by correcting the software miscounts.

    Statistical analysis. Data from for each region and group were the mean sum of counts of the 5 slices/rat for each rat constituting the group. Results are expressed as means ± SEM. Data were evaluated by ANOVA or ANOVA for repeated measures (food intake data) (SAS version 6.11). A post-hoc Tukey’s honestly significant difference test was used to compare between-group means when the ANOVA test was significant. Differences were considered significant at P < 0.05.


   RESULTS
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 RESULTS
DISCUSSION
 LITERATURE CITED
 
When the rats were switched from the NP to the HP diet, d 1 food intake decreased to ~50% (Fig. 1). Food intake then remained at ~80% of the NP intake after habituation. Rats rapidly became habituated to the daily feeding schedule and learned to eat the 2-g preweighed diet sample in 15 min. All CNS studied regions, except the parabrachial nucleus (PBN) and the area postrema (AP), clearly exhibited Fos protein expression (Table 2).



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  		FIGURE 1 Food intake in rats fed a NP diet for 21 d or switched to a HP diet for 2 or 21 d. Values are means ± SEM, n = 8. Means with different letters differ, P < 0.05 (diet effect P < 0.01; time effect P < 0.001; time x diet effect P < 0.001).

 

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  		TABLE 2 Quantification of Fos expression in different CNS regions of rats switched from NP to HP diets1

 
    Fos expression during transition from the NP to the HP diet (NP-d21 vs. HP-d2). Three of the 12 CNS regions studied showed changes in Fos expression in the early phase of the transition from the NP to the HP diet: the arcurate nucleus (ARC), the DMH, and the ACC (P < 0.01) (Table 3). In contrast, the nucleus of the solitary tract (NTS); APC; paracentricular nucleus (PVN); amygdala, cortex (ACO); amygdala, central nucleus (ACN); PBN; and AP were not affected. In the early phase of the transition to a HP diet, Fos expression was significantly increased by 96 and 59% in the DMH and ACC, respectively, and significantly decreased by 51% in the ARC.


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  		TABLE 3 Changes in Fos expression in brain areas of rats switched from NP to HP diets1

 
    Fos expression after habituation to the HP diet (HP-d2 vs. HP-d21). In rats fed the NP-d2 diet, alterations in Fos protein expression were observed in the NTS, ARC, lateral hypothalamus (LH), DMH, ACN, and ACC (P < 0.01) but not in the APC, PVN, ventromedial hypothalamus (VMH), ACO, PBN, or AP. Fos expression was increased by 131 and 69% in the NTS and ARC, and significantly decreased by 47, 43, 42, and 51% in the LH, DMH, ACN, and ACC, respectively. In the APC, LH, DMH, ACN, and ACC, these changes constituted a return to NP-d21 levels.

    Fos expression after habituation to the HP or to the NP diet (NP-d21 vs. HP-d21). In rats fed the HP-d21 diet, only 3 of the 12 areas studied differed significantly: the NTS, the VMH, and the ACO (P < 0.001). Fos expression was increased by 126% in the NTS, and decreased by 30 and 45% in the VMH and ACO, respectively. The NTS showed the most marked increase on d 21, whereas decreases in the VMH and ACO appeared to result from a trend on d 2 (P = 0.1 and 0.08, respectively) and became significant by d 21.


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Assuming that Fos expression provides a reliable marker of neuronal activation (14,15), the present study showed significant modifications in the activity of several CNS areas when rats were switched from NP to HP diets (NP-d21 to HP-d2) and after habituation to the HP diet (HP-d21). It is interesting that the patterns of Fos immunoreactivity were markedly different in the several brain areas studied.

During the transition period (HP-d2 vs. NP-d21), quantification of Fos expression revealed changes in the activity of 3 distinct brain areas: the ARC, the DMH, and the ACC. VMH (P = 0.06) and ACO (P = 0.08) tended to decrease over the course of HP feeding. Fos protein expression was decreased briefly by 51% in the ARC, which was reported to act as a central chemosensor for circulating satiety signals, including leptin and insulin (16). After adaptation (HP-d21 vs. NP-d21), Fos in the ARC returned to NP-d21 levels. Alternatively, the ARC may have responded to the early energy deprivation associated with reduced food intake. Fos protein expression was increased by 96% in the DMH, a brain site previously shown to exhibit cholecystokinin (CCK)-1 receptors, thus being a target for the satiety signal CCK (17). Rats with DMH lesions increased their food intake even more than sham-operated controls in response to food deprivation, thus suggesting that the DMH might be involved in limiting food intake (18); this observation is consistent with our findings. DMH is also associated with protein intake. Fos protein expression was increased in the ACC, which is thought to participate in the central control of food intake (19). Indeed, because the ACC integrates various types of information (cognitive, emotional, energy balance) it is thought to be a site of complex control of ingestive behavior and to be associated with various reinforcers. Interestingly, most of the short-term changes were counterbalanced by long-term habituation processes, reducing the overall differences between the NP and HP diets in the long term. Whether changes observed in the transition period can be attributed solely to the change in dietary protein level remains unclear. It is indeed likely that the observed changes occurring during the transition period from NP to HP diets, which disappeared after habituation, were only partially induced by the increase in protein amount per se but were also due to the change in type of food and may have resulted from the decrease in food intake.

In contrast, after habituation to the HP diet (HP-d21 vs. NP-d21), significant changes in Fos expression consisted in an upregulation in the NTS and a downregulation in the VMH and the ACO. The NTS is the only brain area showing a late and marked upregulation in Fos expression in rats habituated to the HP diet. This is the first report showing activation of the NTS by increased protein intake in freely fed rats. The NTS is a part of the dorsal vagal complex, located in the medulla oblongata; it is the principal recipient of first-order visceral and gustatory afferent information conveyed by the vagus nerve. Information originating from the entire digestive tract (from the mouth to the rectum) is sent to the NTS, which has already been shown to be involved in regulation of food intake–related events such as glucose, lipid, and amino acid ingestion, and the production of satiating effects (20). Its projections to the hypothalamus and the amygdala and its innervation descending from these areas make the NTS a strategically important area in the central control of food intake. In the present study, we did not observe NTS activation during the transition period. This may have resulted from an initial descending inhibition of peripheral input that would be subsequently overridden by an increase in peripheral sensitivity. Several studies indeed reported the occurrence of such a descending inhibition originating either in the amygdala or in the hypothalamus (21–24). Aberrant or abnormal states, such as continuous consumption of a high-fat diet or pathophysiologic states, modulate the vagal sensitivity to nutrients (25). These results show that the NTS and likely the vagus nerve are involved in processing the information received after consumption of high dietary protein. However the precise contribution of the parasympathetic system to the detection of HP intake is not understood. Indeed, the initial translating mechanisms likely to occur within the small intestine have not yet been elucidated.

The other long-term modification observed after habituation to the HP diet was a downregulation of Fos expression in both the VMH and the ACO. Interestingly, the VMH establishes bidirectional projection with the NTS and is the recipient of inputs from the amygdala. The VMH is also thought to play a crucial role in the regulation of food intake because it is a target of many mediators of satiety such as GLP-1, leptin, insulin, dopamine, NPY, CCK, histamine, or interleukin ß (11,25–27). VMH lesions induce obesity (28) but the reported decrease in VMH activity is not actually consistent with this hypothesis. The VMH also influences sympathetic nervous system outflow. Considering that the sympathetic nervous system plays a major role in the control of body metabolism and because the VMH regulates sympathetic outflow, some observed metabolic changes such as a decrease in body fat following HP diet intake could originate in the VMH (29). The amygdala has been studied as a major central region in terms of food intake monitoring; lesions of various components of this complex cause changes in feeding behavior (8,30). The amygdala was shown to establish direct reciprocal connections with the dorsal vagal complex, and especially with the NTS and hypothalamic regions (31). This area is thus likely to be able to receive direct information from changes in the protein content of the diet. Furthermore, it was also established that the amygdala is associated with motivation, sensation reinforcement, and reward networks because it is an important part of the limbic system and has a reciprocal connection with the ACC region. Changes in activity in the amygdala suggest a processing of HP-related information by the limbic system (32).

The present study supports the general hypothesis that central control of food intake in omnivores is associated with peripheral information. Protein ingestion– and metabolism-related information may play a major role in these pathways. Although HP diets provide a strong and reliable model for satiety induction, it is unclear whether the present findings can be integrated into a general model of satiety. The physiologic mechanisms of HP diet–induced depression of food intake are unknown. Video-based behavioral pattern analysis performed in our laboratory showed that HP diet–induced food intake depression was due either to an enhancement of normal physiologic satiety or to poor palatability rather than to the induction of a conditioned taste aversion (4). In addition, we were unable to increase HP diet intake by modifying several orosensory characteristics. For example, adding sucrose to a HP diet, modifying the protein source, or replacing carbohydrates by fat did not reverse food intake depression (33), suggesting thus that the observed changes resulted from the dietary protein content rather than from an alteration of the diet sensory profile. However, additional research using gavage techniques or gastric catheters would allow the collection of useful data that bypassed the oral-sensorial route. Of the 3 macronutrients, protein is likely to play a major role in the emergence of satiety (4,5). Our study showed that the HP diet not only dramatically suppressed food intake in rats but also elicited changes in various CNS areas such as the NTS, the amygdala, and the VMH. Considering the functional characteristics of these areas the present results suggest the following: 1) the involvement of the vagus nerve in conveying the information relative to the quantity of ingested proteins from the site of detection to the CNS; 2) the implication of hypothalamic sites regulating food intake and a putative alteration of sympathetic nervous system activity; 3) the involvement of higher brain function such as memory processing by the limbic system or the food reward system. To refine our understanding of these mechanisms, studies will require determination of the neurochemical pathways involved in the regulation of HP diet ingestion and the actual mechanisms of detection of dietary protein.


   FOOTNOTES
 
2 Abbreviations used: ACC, nucleus accumbens; ACN, amygdala, central nucleus; ACO, amygdala, cortex; AP, area postrema; APC, anterior piriform cortex; ARC, arcuate nucleus; CCK, cholecystokinin; CNS, central nervous system; DAB, diaminobenzidine; DMH, dorsomedial hypothalamus; HP, high-protein diet; HP-d2, group of rats habituated to NP and fed HP for 2 d; HP-d21, group of rats habituated to HP; LH, lateral hypothalamus; NP, normal-protein diet; NP-d21, group of rats habituated to NP; NTS, nucleus of the solitary tract; PBN, parabrachial nucleus; P/E, percentage of total energy made up with protein; PVN, paraventricular nucleus; VMH, ventromedial hypothalamus. Back

Manuscript received 30 October 2004. Initial review completed 16 December 2004. Revision accepted 4 March 2005.


   LITERATURE CITED
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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