Behavioral satiety sequence: an experimental model for studying feeding behavior

Sequência comportamental de saciedade: um modelo experimental para o estudo do comportamento alimentar

REVIEW REVISÃO

Behavioral satiety sequence: an experimental model for studying feeding behavior

Sequência comportamental de saciedade: um modelo experimental para o estudo do comportamento alimentar

Lisiane dos Santos Oliveira^I; Sandra Lopes de Souza^II; Raul Manhães-De-Castro^III

^IUniversidade Federal de Pernambuco, Centro Acadêmico de Vitória. R. Alto do Reservatório, s/n., Bela Vista, 55608-580, Vitória de Santo Antão, PE, Brasil

^IIUniversidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Anatomia. Recife, PE, Brasil

^IIIUniversidade Federal de Pernambuco, Centro de Ciências da Saúde, Departamento de Nutrição. Recife, PE, Brasil

^{Correspondence to}

ABSTRACT

Feeding behavior is controlled by interactions between psychobiological and physiological systems. In rats, there is a sequence in the feeding behavior that is characterized by similar movements at the beginning and end of a meal, known as the behavioral satiety sequence. In the sequence, eating is followed by grooming and other activities, and ends with resting. The objective of this systematic review is to evaluate the use of the behavioral satiety sequence as an experimental model for the study of feeding behavior. A systematic search of the electronic databases MedLine, Lilacs, SciELO, Cochrane Library and PubMed was done from November 2007 to January 2008, using combinations of the keywords "behavioral," "satiety" and "sequence". Ninety articles were found and, of these, fifteen articles were selected for the review. The studies demonstrated the efficacy of using behavioral satiety sequence to evaluate the effects of some types of manipulations on feeding behavior. With this study method it was also possible to observe different factors that can interfere with feeding behavior, such as sedation, malaise or intake inhibition, by increasing satiety. Behavioral satiety sequence offers solid tools for gaining a better understanding of how treatment can influence feeding behavior.

Indexing terms: Feeding behavior. Resting. Satiety response.

RESUMO

O comportamento alimentar é controlado por interações entre sistemas psicobiológicos e fisiológicos. Em ratos, existe uma sequência no comportamento alimentar que é caracterizada por movimentos similares no início e no término de uma refeição, conhecida como sequência comportamental de saciedade. Na sequência, o ato de comer é seguido pela limpeza e outra atividades, terminando com o descanso. O objetivo dessa revisão sistemática é avaliar o uso da sequência comportamental de saciedade como um modelo experimental para o estudo do comportamento alimentar. Uma busca sistemática das bases de dados MedLine, Lilacs, SciELO, Biblioteca Cochrane e PubMed foi realizada, no período de novembro de 2007 a janeiro de 2008, usando combinações das palavras chaves "behavioral", "satiety" e "sequence". Noventa artigos foram encontrados e, desses, quinze artigos foram selecionados para a revisão. Os estudos mostraram a eficácia do uso da sequência comportamental de saciedade para a avaliação dos efeitos de alguns tipos de manipulações sobre o comportamento alimentar. Com esse método de estudo, também é possível observar diversos fatores que podem intervir no comportamento alimentar, assim como sedação, mal-estar ou inibição do consumo por aumento da saciedade. A sequência comportamental de saciedade oferece sólidas ferramentas para obter um entendimento melhor de como um tratamento pode influenciar o comportamento alimentar.

Termos de indexação: Comportamento alimentar. Descanso. Resposta de saciedade.

INTRODUCTION

Appetite control is based on a psychobiological system and reflects the synchronous operation of events and processes involved with this system¹. An interaction exists between psychological events (hunger perception, cravings, hedonic sensations), behavioral operations (intake of meals, snacks, energy and macronutrients), peripheral physiologic and metabolic events, and the levels of neurotransmitter and metabolic interactions in the brain that control feeding behavior².

The feeding behavior of animals is an adaptive response, arising from demands of the internal environment and is modulated by limitations imposed by the external environment³. Neural events trigger and guide behavior, but each behavioral act involves a response in the peripheral physiological system¹. These physiological responses are termed satiety signals, and can be represented by the satiety cascade¹.Some concepts must be defined to understand feeding behavior better. Satiety involves the events subsequent to food intake that suppress hunger and maintain an inhibition toward eating for a particular period of time while hunger can be regarded as the need to eat or a period in which satiety signals are absent¹. Between hunger and satiety there is satiation, a group of processes that determine meal termination¹. The coordinated effects of satiation and satiety control the size and frequency of eating episodes, thereby defining the eating pattern¹.

Studies have demonstrated that some behaviors in animals follow specific patterns^4,5. Thus, after eating, an adult rat presents a period of grooming and locomotor activity⁵. After this period, the animal rests or sleeps⁴. Following these observations, a behavioral sequence was identified that is associated with satiety, because the cessation of eating is not a sufficient condition for the complete appearance of this behavioral sequence⁶. Thus the sequence was named Behavioral Satiety Sequence (BSS)⁶.

In 1975, the BSS was used for the first time as an experimental model for the study of satiety⁶. This work confirmed the association of postingestive behavior with satiety, and it is still considered a landmark for the consolidation of BSS as a technique for the study of feeding behavior.

In rodents, BSS is characterized as an eating phase, followed by grooming and locomotor activities and ending with a resting phase^6,7. Eating itself is characterized by biting, gnawing, or swallowing food directly from a dish or from the front paws^6,7. This action is one of the elements of feeding behavior that is related to the biological need of getting nutrients.

Grooming is characterized by licking of the body, feet and genitals, by scratching the coat or head with the hind leg, by stroking whiskers with the paws and biting the tail^6,7. These actions normally occur after eating⁷. Locomotion involves movements with the participation of the four limbs and rearing (front paws raised from the cage floor, either supported against a wall or free standing)^6,7. Locomotor activity is related to exploratory behavior⁸. It consists of acts and postures that allow the animal to acquire information and to become familiar with its environment⁸. Changes of activities related to BSS can interfere with feeding behavior⁶. The increased duration and/or frequency of non-feeding activities associated with BSS can delay the start of the resting period and fragment eating into numerous, short episodes^3,7.

Resting is characterized by inactivity. The animal sits or lies in a relaxed position with its head curled close to the body or resting against the floor^6,7. Resting is the final posture assumed in the BSS^6,7. The appearance of the resting posture in BSS is a condition caused by satiety⁷. This fact was demonstrated by changes of palatability, reduced food intake and because resting does not occur⁹. It has also been verified that the onset of resting can be anticipated by the prefeeding period¹⁰.Drug-induced changes can alter BSS and make resting occur before eating⁶.

The objective of this systematic review was to evaluate, through studies published in indexed journals, the efficiency of the BSS method for studying feeding behavior, as well as what type of behavioral interference related to satiety can be highlighted with the BSS method, since the study of food intake alone will not allow such verification.

METHODS

A systematic search of the literature was done from November 2007 to January 2008 in the electronic databases MedLine (National Library of Medicine), Lilacs (Literatura Latino-americana e do Caribe em Ciências da Saúde), SciELO (Scientific Electronic Library Online), Cochrane Library and PubMed. This search focused on studies published from 1975 to 2008 that used BSS. The literature search used combinations of the keywords "behavioral", "satiety" and "sequence". In order to define the literature for this review, the following inclusion criteria were established: a) studies that used the BSS method; b) studies with rats or mice; c) articles that considered the time when BSS was evaluated, such as eating, grooming and/or resting behavior durations. Articles that did not disclose eating, grooming and/or resting behavior durations or that had problems in the statistical analyses, such as no significance values or no confidence intervals, were excluded.

RESULTS AND DISCUSSION

The initial search of the databases returned fifteen articles in MedLine, two articles in the Cochrane Library and ninety articles in PubMed. The two articles of the Cochrane Library were discarded because they did not concern BSS. The fifteen articles found in Medline were also present in PubMed. Of the ninety articles found in PubMed, thirty were discarded after analysis of the abstracts because they did not concern BSS. After reading the abstracts, sixty articles were selected and after complete analysis of each article, only fifteen articles met the inclusion criteria mentioned earlier. The results tabulated for this study were the murine species, phase of the light/dark cycle, duration of BSS assessment, type of diet or treatment and method of administration, amount of food consumed and duration of eating, grooming and resting behaviors. The duration of eating, grooming and resting behaviors were presented as means or percentage ± standard deviation. The articles were categorized according to type of manipulation: nutritional, pathological or pharmacological, and are summarized in Tables 1, 2 and 3, respectively.

All articles used analysis of variance to compare the groups. The studies demonstrated the ample applicability and usefulness of BSS for evaluating feeding behavior. In particular, these studies show that BSS analysis is a simple method used for establishing the microstructure of feeding. That is, to define the duration and/or frequency of each behavior associated with food intake.

In the first category of studies where the effects of nutritional manipulations on the temporal feeding pattern were examined (Table 1), it was clear how hunger and satiety states¹⁰, diet palatability⁹, and satiation power of the ingested diet¹¹ affect feeding behavior. Thus, adulteration of food with quinine⁹, a bitter substance, reduced food intake without affecting eating duration and abolished the resting behavior usually observed at the end of BSS. Since satiety is associated with sleeping or inactivity, the absence of resting indicates lack of satiation. This observation underlies the fact that the taste of food is a crucial determinant of feeding and that this factor must be considered when the anorexic or orexigenic properties of a drug are studied or when the characterization of a drug response involves its administration through drinking water.

BBS has also been used to examine the effect of a high-protein diet on satiety¹¹, and in particular on food intake, the rate of feeding and the relation between food intake and eating duration. In this study, animals were fed either standard chow or a high-protein diet and their feeding behavior was evaluated daily. On the first day, the animals fed the high-protein diet exhibited a reduction in food intake and rate of feeding, as well as an increased eating duration and a decreased resting duration. From the second to the fourteenth day, no differences between the two groups in the temporal BSS pattern were observed. The reduced resting duration in the first day indicated that a high-protein diet delays the appearance of satiety but this initial aversion to the high-protein diet is followed by adaptation.

Finally, it has been demonstrated that the interval between meals can affect food intake and the appearance of satiation⁹. Specifically, it was observed that the longer the fasting period, the greater the food intake and the duration of eating, and that the longer the pre-feeding period, the smaller the latency to begin eating and the feeding duration. These results indicate that a smaller interval of time between meals can reduce the motivation to eat the next meal. Using this experimental approach, one can obtain information about the temporal display of feeding behavior, and identify the level of control in which individual behaviors are affected by nutritional manipulations.

In the second study category (Table 2), BSS was used to analyze how a pathological state can interfere with food intake. In one of these studies¹², the effects of muramyl dipeptide on feeding behavior were analyzed. Muramyl dipeptide is the minimally active subunit of bacterial peptidoglycan, which is abundantly released during infections by gram-positive bacteria^13,14, and has been associated with reduced food intake during infection¹⁵. In this study, none of the parameters of BSS, including the amount of ingested food, eating duration and feeding rate were altered within the first two hours after the administration of muramyl dipeptide. However, three hours after the administration of muramyl dipeptide there was a reduction in grooming duration and prolonged resting period. These behavioral changes are similar to those that appear during illness. This study also evaluated the cumulative food intake over a 24-hours period. This analysis demonstrated that the inhibitory effects of muramyl dipeptide on food intake extend from the third to the tenth hour after its administration. Collectively, these data suggest that the hypophagic effect of illness induced by a bacterial infection results from a change in the physiological mechanisms involved in the regulation of satiety.

In relation to the changes in feeding behavior associated with a pathological state, it has also been observed that the discomfort caused by the administration of Lithium Chloride (LiCl) is related to diminished food intake, reduced grooming duration and longer eating period¹⁶. Reduced food intake correlated with increased eating duration, thereby resulting in reduced feeding rate. LiCl-induced anorexia is associated with behavioral signs of malaise such as reduced activity, low food intake rate and BSS disruption. These observations corroborate previous studies¹², indicating that anorexia is related to the discomfort caused by sickness.

BSS has been extensively used in pharmacological studies that aimed to identify new therapeutic targets for the treatment of eating disorders and its consequences, such as obesity, as well as to get an insight into the mechanism involved in the control of feeding behavior, both at the central and peripheral levels (Table 3). In relation to the first point, it has been recently demonstrated that orexins participate in the regulation of feeding behavior by stimulating food intake¹⁶. Orexin-A and orexin-B are neuropeptides derived from prepro-orexin. Both peptides exert their actions through the activation of orexin-1 and orexin-2 receptors but orexin-A binds with greater affinity to the orexin-1 receptor¹⁷. Intracerebroventricular administration of orexin-A leads to increased food intake. The fact that this hyperphagic effect is not associated with increased meal duration indicates that the orexigenic properties of orexin-A are due to its capacity to increase feeding rate¹⁸. On the other hand, the intraperitoneal administration of SB-334867, an antagonist of the orexin-1 receptor, reduces food intake and eating duration and increases resting duration^16,19. These results indicate that orexin stimulates food intake through its interaction with orexin-1 receptors.

The intestinal hormone cholecystokinin is a satiety signal with anorexic effects^7,20-22. The administration of an equi-anorectic dose of the natural satiety-related signal cholecystokinin octapeptide (CCK-8S) induced reduced food intake, along with increased latency to begin eating, increased eating and resting duration, and reduced grooming duration. Collectively, these observations indicate that cholecystokinin reduces satiety before eating begins and stimulates satiety after eating begins. Analysis of the effects of other pharmacological or nutritional manipulations on the pattern of BSS induced by the administration of cholecystokinin might be of interest for the dissection of other variables related to satiety.

Endogenous opioids are also involved in the regulation of appetite. Systemic or central administration of these peptides induces hyperphagia²³. The physiological mechanisms underlying the orexigenic effects of opioids were investigated by the use of naloxone, an opioid receptor antagonist¹⁸. The administration of this compound was shown to reduce both food intake and eating duration in control rats, without affecting the latency to start eating. Thus, opioids clearly regulate the satiety process but, in disagreement with a generally accepted idea, they do not seem to be involved in the motivation to eat.

BSS has also been used to analyze the anorexic effects of the YY3-36 peptide^24,25. This peptide is released into the gastrointestinal tract after meals²⁶. Examination of the BSS pattern after the administration of the YY3-36 peptide showed significant reductions in food intake and in eating duration. In addition, there was as an increase in resting duration, which is consistent with delayed onset of satiety. These results indicate that the YY3-36 peptide reduces food intake because it promotes satiety²⁷. The stimulation of type 2 presynaptic receptors for neuropeptide Y (NPY) inhibits the release of NPY and GABA from hypothalamic arcuate nucleus neurons. Given that NPY is a potent orexigenic peptide and that YY3-36 peptide also stimulates NPY type-2 receptors²⁴, the possibility exists that the inhibitory effects of YY3-36 on food intake are mediated by NPY. In agreement with this hypothesis, the administration of a Y2-receptor antagonist alone did not alter BSS but prevented the anorexic effect of YY3-36²⁷.

BSS has been extensively used for the study of the effects of serotonin on food intake. Although all the studies performed so far agree that the inhibitory effects of serotonin on food intake are related to its capacity to advance satiety, some discordant results exist in relation to how serotonin affects the other behavioral components of the feeding microstructure. For example, the administration of fluoxetine, a selective serotonin reuptake inhibitor, reduces food intake but does not change eating duration or increases resting period²⁸. In contrast, the administration of fenfluramine, a serotonin reuptake inhibitor which also stimulates the release of serotonin, leads to an inhibition of food intake which is associated with reduced eating duration and increased resting period²⁹. Moreover, metergoline, a serotoninergic receptor antagonist, does not alter food intake or eating duration, but it does increase the resting period²⁸. When fluoxetine was administered together with metergoline, eating and resting duration increased but food intake did not change²⁸, indicating that metergoline inhibited the effect of fluoxetine on the inhibition of food intake.

These controversial results can be explained by the fact that serotonin interacts with 14 different receptors which have been classified into different families according to their pharmacological, molecular and functional properties. Among these, serotonin 5-HT1B and 5-HT2C receptors have been specifically recognized as mediators of serotonin-induced satiety^29,30. Thus, RU-24969, an agonist of the 5-HT-1A and 5-HT-1B receptors, reduces food intake and eating duration without changing the resting period³¹. Similarly, the administration of CP-94,253, a selective 5-HT1B receptor agonist, reduced food intake and eating and grooming durations but, in contrast to the administration of RU-24969, increased resting duration³². These findings clearly demonstrate that 5-HT-1B receptors modulate the inhibitory effects of serotonin on food intake.

On the other hand, initial studies indicated that the administration of MK-212, a 5-HT-2 receptor agonist, reduces food intake and increases resting duration but does not change eating duration³⁰. These data indicate that serotonin 5-HT-2 receptors regulate feeding behavior through the stimulation of satiety. Subsequent studies with RO-60-0175 and VER23779, two selective 5-HT-2C receptor agonists, confirmed that the specific stimulation of 5-HT2C receptors inhibits food intake by reducing feeding time and increasing resting time^29,33. Collectively, these and other analyses of the BSS in association with pharmacological studies using selective serotonin receptor compounds, indicate that the anorexic action of serotonin is mediated by separate receptor subtypes. Thus, while the reduced meal size consecutive to the administration of serotonin would depend on the stimulation 5-HT1B receptors, the reduction in feeding rate would result from the selective stimulation of 5-HT2C receptors.

For BSS analysis, all the examined studies relied on a standard procedure in which a fooddeprived animal is placed in an observation arena with ad libitum access to food and water for a period of 45-60 min. Food deprivation is used to obtain a high feeding baseline while the objective of the observation arena is to provide a larger enclosure than the animal's house-cage to allow the expression of all the BSS behavioral parameters. The experimental protocol used differed, however, between the different laboratories in some respects. These included the phase of the light/dark cycle in which the test was performed, the duration of the fasting period and how the behavioral data were analyzed and presented.

Most living organisms exhibit behavioral and physiological rhythms, including those associated with sleep, feeding and energy homeostasis. Therefore, the expression of BSS can vary depending on the phase of the light/dark cycle in which the analysis is performed. Initially, the BSS was monitored essentially during the light phase⁷, but more recently analysis of the BSS during the dark phase has been preferred^18,19. In the first studies in which BSS was analyzed during the light phase, the animals were submitted to a fasting period of 17-20 hours^3,7. The objective of this procedure was to reduce the eating latency and to stimulate the onset of the characteristic BSS behaviors. However, rats are nocturnal and, consequently, most of its activity, including eating, occurs during the dark cycle. During this phase, rats consume up to 80% of their daily food intake³⁴. Thanks to the development of monitoring technology, it is possible to document BSS during the dark phase using special video recorders and red light. The use of this methodology allows not only BSS analysis under more natural conditions, but also has the advantage of reducing the fasting period. Currently, studies done during the dark phase usually use a four-hour food deprivation period^6,28,30,35.

The data gathered in these studies were analyzed in different ways. Some authors calculated the frequency of each behavior, e.g., the number of episodes of each behavioral category per time bin (usually 5min), whereas other authors expressed the duration of each behavior in relation to the total length of the observation period (45-60min).

Only six articles of the fifteen articles presented data on feeding latency (Tables 1, 2 and 3). That is, the interval of time between the presentation of food and the moment at which the animal actually starts eating. Pre-satiated rats present longer latency periods to begin feeding⁹. Since food ingestion reduces the stimulation to start a new meal, feeding latency can be a measure of the animal's motivation to eat.

Food intake is also an important factor for the interpretation of BSS. By the measurement of food intake and the duration of eating, that is, the time the animal actually spends consuming food, the feeding rate can be determined by calculating the ratio between food intake (g) and eating duration (min). It is also possible to quantify the mean intake per eating episode through quantification of the relationship between food intake (g) and the number of eating episodes.

CONCLUSION

BSS is a noninvasive, inexpensive and highly efficient method for analyzing feeding behavior. The effects of pharmacological and nutritional manipulations on the natural physiological regulation of food intake can be evaluated using BSS. It is regrettable that many studies that aim to characterize the orexigenic or anorexigenic properties of a drug use the amount of ingested food as the only feeding behavior variable. Although a reduction or an increase in food ingestion reflects an effect on appetite, the measurement of food intake alone does not allow the determination of whether these changes are due to a change of the physiological mechanisms regulating food intake or to nonspecific effects, such as sedation, hyperactivity, malaise or enhanced satiety. BSS is a solid experimental tool for improving our understanding of the complex psychological and physiological processes involved in the regulation of feeding behavior.

CONTRIBUTORS

All authors contributed substantially to the paper, including literature review, organization of the manuscript, translation and critical review.

22. Halford JC, Boyland EJ, Cooper GD, Dovey TM, Smith CJ, Williams N, et al. Children's food preferences: effects of weight status, food type, branding and television food advertisements (commercials). Int J Pediatr Obes. 2007:1-8. doi: 10.1080/17477160701645152.

23. Bodnar RJ. Endogenous opioids and feeding behavior: a 30-year historical perspective. Peptides. 2004;25(4):697-725. doi: 10.1016/j.peptides.2004.01.006.

24. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, et al. Gut hormone PYY (3-36) physiologically inhibits food intake. Nature. 2002;418(6898):650-4. doi: 10.1038/nature00887.

25. Chelikani PK, Haver AC, Reidelberger RD. Intravenous infusion of peptide YY(3-36) potently inhibits food intake in rats. Endocrinology. 2005;146(2):879-88. doi: 10.1210/en.2004-1138.

26. Adrian TE, Ferri GL, Bacarese-Hamilton AJ, Fuessl HS, Polak JM, Bloom SR. Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology. 1985;89(5):1070-7. PII: 0016-5085(85)90211-2.

27. Scott V, Kimura N, Stark JA, Luckman SM. Intravenous peptide YY3-36 and Y2 receptor antagonism in the rat: effects on feeding behaviour. J Neuroendocrinol. 2005;17(7):452-7. doi: 10.11 11/j.1365-2826.2005.01330.x.

28. Halford JC, Blundell JE. Metergoline antagonizes fluoxetine-induced suppression of food intake but not changes in the behavioural satiety sequence. Pharmacol Biochem Behav. 1996;54(4):745-51. doi: 10.1016/0091-3057(95)02228-7.

29. Hewitt KN, Lee MD, Dourish CT, Clifton PG. Serotonin 2C receptor agonists and the behavioural satiety sequence in mice. Pharmacol Biochem Behav. 2002;71(4):691-700. doi: 10.1016/S0091-3 057(01)00709-2.

30. Halford JC, Lawton CL, Blundell JE. The 5-HT2 receptor agonist MK-212 reduces food intake and increases resting but prevents the behavioural satiety sequence. Pharmacol Biochem Behav. 1997;56(1):41-6. doi: 10.1016/S0091-3057(96)00152-9.

31. Halford JC, Blundell JE. The 5-HT1B receptor agonist CP-94,253 reduces food intake and preserves the behavioural satiety sequence. Physiol Behav. 1996;60(3):933-9. doi: 10.1016/0031-93 84(96)00073-X.

32. Lee MD, Kennett GA, Dourish CT, Clifton PG. 5-HT1B receptors modulate components of satiety in the rat: behavioural and pharmacological analyses of the selective serotonin1B agonist CP-94,253. Psychopharmacology (Berlin). 2002;164(1):49-60. doi: 10.1007/s00213-002-1162-7.

33. Somerville EM, Horwood JM, Lee MD, Kennett GA, Clifton PG. 5-HT(2C) receptor activation inhibits appetitive and consummatory components of feeding and increases brain c-fos immunoreactivity in mice. Eur J Neurosci. 2007;25(10):3115-24. doi: 10.1111/j.1460-9568.2007.05567.x.

34. Vachon C, Savoie L. Circadian variation of food intake and digestive tract contents in the rat. Physiol Behav. 1987;39(5):629-32. doi: 10.1016/0031-93 84(87)90164-8.

35. Reeves PG, Nielsen FH, Fahey GC, Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123(11):1939-51

Received on: 23/3/2010

Final version resubmitted on: 13/1/2011

Approved on: 22/2/2011

• 1. Blundell JE, Goodson S, Halford JC. Regulation of appetite: role of leptin in signalling systems for drive and satiety. Int J Obes Relat Metab Disord. 2001;25(Suppl 1):S29-34
• 2. Blundell J. Pharmacological approaches to appetite suppression. Trends Pharmacol Sci. 1991;12(4): 147-57. doi: 10.1016/0165-6147(91)90532-W.
• 3. Blundell JE, Rogers PJ, Hill AJ. Behavioural structure and mechanisms of anorexia: calibration of natural and abnormal inhibition of eating. Brain Res Bull. 1985;15(4):371-6. doi: 10.1016/0361-9230(85)90 004-8.
• 4. Bindra D, Blond J. A time-sample method for measuring general activity and its components. Can J Psychol. 1958;12(2):74-6.
• 5. Bolles RC. Grooming behavior in the rat. J Comp Physiol Psychol. 1960;53(3):306-10.
• 6. Halford JC, Wanninayake SC, Blundell JE. Behavioral satiety sequence (BSS) for the diagnosis of drug action on food intake. Pharmacol Biochem Behav. 1998;61(2):159-68. doi: 10.1016/S0091-3 057(98)00032-X.
• 7. Antin J, Gibbs J, Holt J, Young RC, Smith GP. Cholecystokinin elicits the complete behavioral sequence of satiety in rats. J Comp Physiol Psychol. 1975;89(7):784-90. doi: 10.1037/h0077040.
• 8. Berlyne DE, Koenig ID, Hirota T. Novelty, arousal, and the reinforcement of diversive exploration in the rat. J Comp Physiol Psychol. 1966;62(2):222-6. doi: 10.1037/h0023681.
• 9. Ishii Y, Blundell JE, Halford JC, Rodgers RJ. Palatability, food intake and the behavioural satiety sequence in male rats. Physiol Behav. 2003;80(1): 37-47. doi: 10.1016/S0031-9384(03)00207-5.
• 10. Ishii Y, Blundell JE, Halford JC, Rodgers RJ. Effects of systematic variation in presatiation and fasting on the behavioural satiety sequence in male rats. Physiol Behav. 2003;79(2):227-38. doi: 10.1016/S0031-9384(03)00066-0.
• 11. Bensaid A, Tome D, L'Heureux-Bourdon D, Even P, Gietzen D, Morens C, et al A high-protein diet enhances satiety without conditioned taste aversion in the rat. Physiol Behav. 2003;78(2):311-20. doi: 10.1016/S0031-9384(02)00977-0.
• 12. Fosset S, Fromentin G, Rampin O, Lang V, Mathieu F, Tome D. Pharmacokinetics and feeding responses to muramyl dipeptide in rats. Physiol Behav. 2003;79(2):173-82. doi: 10.1016/S0031-9384(03)000 65-9.
• 13. Krueger JM, Majde JA. Microbial products and cytokines in sleep and fever regulation. Crit Rev Immunol. 1994;14(3-4):355-79.
• 14. Martin JR, Bos M, Jenck F, Moreau J, Mutel V, Sleight AJ, et al 5-HT2C receptor agonists: pharmacological characteristics and therapeutic potential. J Pharmacol Exp Ther. 1998;286(2):913-24. doi: 002 2-3565/98/2862-0913$03.00/0.
• 15. Langhans W. Bacterial products and the control of ingestive behavior: clinical implications. Nutrition. 1996;12(5):303-15. doi: 10.1016/S0899-9007(96) 80052-9.
• 16. Ishii Y, Blundell JE, Halford JC, Upton N, Porter R, Johns A, et al Differential effects of the selective orexin-1 receptor antagonist SB-334867 and lithium chloride on the behavioural satiety sequence in rats. Physiol Behav. 2004;81(1):129-40. doi: 10.1016/j.physbeh.2004.01.009.
• 17. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, et al Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell. 1998;92(5):1 page following 696. doi: 10.1016/S0092-8674(00)80949-6.
• 18. Tallett AJ, Blundell JE, Rodgers RJ. Night and day: diurnal differences in the behavioural satiety sequence in male rats. Physiol Behav. 2009;97(1): 125-30. doi: 10.1016/j.bbr.2007.10.005.
• 19. Ishii Y, Blundell JE, Halford JC, Upton N, Porter R, Johns A, et al Satiety enhancement by selective orexin-1 receptor antagonist SB-334867: influence of test context and profile comparison with CCK-8S. Behav Brain Res. 2005;160(1):11-24. doi: 10.10 16/j.bbr.2004.11.011.
• 20. Gibbs J, Young RC, Smith GP. Cholecystokinin elicits satiety in rats with open gastric fistulas. Nature. 1973;245(5424):323-5. doi: 10.1038/245323a0.
• 21. Gibbs J, Young RC, Smith GP. Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol. 1973;84(3):488-95.

Publication Dates

• Publication in this collection
  30 Nov 2011
• Date of issue
  Aug 2011

History

• Accepted
  22 Feb 2011
• Received
  23 Mar 2010