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Effects of bilateral anterior agranular insula lesions on food anticipatory activity in rats

Title:

Effects of bilateral anterior agranular insula lesions on food anticipatory activity in rats

Gavrila, Alex M, Hood, Suzanne, Robinson, Barry and Amir, Shimon (2017) Effects of bilateral anterior agranular insula lesions on food anticipatory activity in rats. PLOS ONE, 12 (6). e0179370. ISSN 1932-6203

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Official URL: http://dx.doi.org/10.1371/journal.pone.0179370

Abstract

Food anticipatory activity (FAA) refers to a daily rhythm of locomotor activity that emerges under conditions of food restriction, whereby animals develop an intense, predictable period of activity in the few hours leading up to a predictable, daily delivery of food. The neural mechanisms by which FAA is regulated are not yet fully understood. Although a number of brain regions appear to be involved in regulating the development and expression of FAA, there is little evidence to date concerning the role of the anterior agranular insular cortex (AICa). The AICa plays a critical role in integrating the perception of visceral states with motivational behaviour such as feeding. We assessed the effect of bilateral electrolytic or ibotenic acid lesions of the AICa on FAA in male Wistar rats receiving food for varying lengths of time (2 h, 3 h, or 5 h) during the middle of the light phase (starting at either ZT4 or ZT6). Contrary to our initial expectations, we found that both electrolytic and ibotenic acid lesions significantly increased, rather than decreased, the amount of FAA expressed in lesioned rats. Despite increased FAA, lesioned rats did not eat significantly more during restricted feeding (RF) periods than control rats. Similar to controls, AlCa-lesioned rats showed negligible anticipatory activity to a restricted treat suggesting that the increased anticipatory activity in lesioned rats is associated with food restriction, rather than the appetitive value of the meal. Monitoring behaviour in an open field indicated that increased FAA in AlCa-lesioned rats was not explained by a general increase in locomotor activity. Together, these findings suggest that the AICa contributes to the network of brain regions involved in FAA.

Divisions:Concordia University > Faculty of Arts and Science > Psychology
Item Type:Article
Refereed:Yes
Authors:Gavrila, Alex M and Hood, Suzanne and Robinson, Barry and Amir, Shimon
Journal or Publication:PLOS ONE
Date:8 June 2017
Digital Object Identifier (DOI):10.1371/journal.pone.0179370
ID Code:982599
Deposited By: DANIELLE DENNIE
Deposited On:08 Jun 2017 19:50
Last Modified:18 Jan 2018 17:55

References:

1. Boulos Z, Terman M. Food availability and daily biological rhythms. Neurosci & Behav Rev. 1980; 4:119–131.

2. Stephan FK, Swann JK, Sisk CL. Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behav Neural Biol. 1979; 25:346–363. pmid:464979

3. Mistlberger RE. Circadian food-anticipatory activity: Formal models and physiological mechanisms. Neurosci & Biobehav Rev. 1994; 18:171–195.

4. Storlien LH, Albert DJ. The effect of VMH lesions, lateral cuts and anterior cuts of food intake, activity level, food motivation, and reactivity to taste. Physiol Behav. 1972; 9:191–197. pmid:4569944

5. Krieger DT. Ventromedial hypothalamic lesions abolish food-shifted circadian adrenal and temperature rhythmicity. Endocrinology. 1980; 106:649–654. pmid:7353535

6. Inouye ST. Ventromedial hypothalamic lesions eliminate anticipatory activities of restricted daily feeding schedules in the rat. Brain Res. 1982; 250:183–187. pmid:7139315

7. Mistlberger RE, Rechtschaffen A. Recovery of anticipatory activity to restricted feeding in rats with ventromedial hypothalamic lesions. Physiol Behav. 1984; 33:227–335. pmid:6505064

8. Gooley JJ, Schomer A, Saper CB. The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci. 2006; 9:398–407. pmid:16491082

9. Mistlberger RE, Rusak B. Food-anticipatory circadian rhythms in rats with paraventricular and lateral hypothalamic ablations. J Biol Rhythms. 1988; 3:277–291.

10. Crawley JN, Kiss JZ. Paraventricular nucleus lesions abolish the inhibition of feeding induced by systemic cholecystokinin. Peptides. 1985; 6:927–935. pmid:4080609

11. Landry GJ, Yamakawa GRS, Mistlberger RE. Robust food anticipatory circadian rhythms in rats with complete ablation of the thalamic paraventricular nucleus. Brain Res. 2007; 1141:108–118. pmid:17296167

12. Mistlberger RE, Mumby DG. The limbic system and food-anticipatory circadian rhythms in the rat: ablation and dopamine blocking studies. Behav Brain Res. 1992; 47:159–168. pmid:1590946

13. Gallardo CM, Darvas M, Oviatt M, Chang CH, Michalik M, et al. Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice. eLife. 2014; 3:e03781. pmid:25217530

14. Recabarren MP, Valdés JL, Farías P, Serón-Ferré M, Torrealba F. Differential effects of infralimbic cortical lesions on temperature and locomotor activity responses to feeding rats. Neuroscience. 2005; 134:1413–1422. pmid:16039788

15. Davidson AJ, Cappendijk SLT, Stephan FK. Feeding-entrained circadian rhythms are attenuated by lesions of the parabrachial region in rats. Am J Physiol Regul Integr Comp Physiol. 2000; 278:R1296–R1304. pmid:10801300

16. Crawley JN, Schwaber JS. Abolition of the behavioral effects of cholecystokinin following bilateral radiofrequency lesions of the parvocellular subdivision of the nucleus tractus solitarius. Brain Res. 1984; 295:289–299. pmid:6713189

17. Davidson AJ, Aragona BJ, Houpt TA, Stephan FK. Persistence of meal-entrained circadian rhythms following area postrema lesions in the rat. Physiol & Behav. 2001; 74:349–354.

18. Mendoza J, Pévet P, Felder-Schmittbuhl M-P, Bailley Y, Challet E. The cerebellum harbors a circadian oscillator involved in food anticipation. J Neurosci. 2010; 30:1894–1904. pmid:20130198

19. Davidson AJ, Aragona BJ, Werner RM, Schroeder E, Smith JC, et al. Food-anticipatory activity persists after olfactory bulb ablation in the rat. Physiol & Behav. 2001; 72:231–235.

20. Craig AD. Significance of the insula for the evolution of human awareness of feelings from the body. Ann NY Acad Sci. 2011; 1225:72–82. pmid:21534994

21. Saper CB. Convergence of autonomic and limbic connections in the insular cortex of the rat. J Comp Neurol. 1982; 210:163–173. pmid:7130477

22. Allen GV, Saper CB, Hurley KM, Cechetto DF. Organization of visceral and limbic connections in the insular cortex of the rat. J Comp Neurol. 1991; 311:1–16. pmid:1719041

23. Reynolds SM, Zahm DS. Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci. 2005; 25:11575–11767.

24. Frank S, Kullmann S, Veit R. Food related processes in the insular cortex. Frontiers in Hum Neuroscience. 2013; 7:1–6.

25. Yamamoto T, Matsuo R, Kawamura Y. Localization of cortical gustatory area in rats and its role in taste discrimination. J Neurophysiol. 1980; 44:440–455. pmid:7441309

26. Jarrard LE. On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. J Neurosci Methods. 1989; 29:251–259. pmid:2477650

27. Verwey M, Khoja Z, Stewart J, Amir S. Differential regulation of the expression of Period2 protein in the limbic forebrain and dorsomedial hypothalamus by daily limited access to highly palatable food in food-deprived and free-fed rats. Neuroscience. 2007; 147:277–285. pmid:17544223

28. Mendoza J, Angeles-Castellanos M, Escobar C. A daily palatable meal without food deprivation entrains the suprachiasmatic nucleus of rats. Euro J Neurosci. 2005; 22:2855–2862.

29. Watson RE Jr, Wiegand SJ, Clough RW, Hoffman GE. Use of cryoprotectant to maintain long-term immunoreactivity and tissue morphology. Peptides. 1986; 7:155–159.

30. Mauchly JW. Significance Test for sphericity of a normal n-variate distribution. Ann of Math Stat. 1940; 11:204–209.

31. Levene H. Robust tests for equality of variances. In Olkin I, Ghurye SG, Hoeffding W, Madow WG, Mann HB (eds). Contributions to probability and statistics. 1960; 278–292.

32. Greenhouse SW, Geisser S. On methods in the analysis of profile data. Psychometrika. 1959; 24:95–112.

33. Honma K-I, von Goetz C, Aschoff J. Effects of restricted daily feeding on freerunning circadian rhythms in rats. Physio & Behav. 1983; 30:905–913.

34. Stephan FK, Becker G. Entrainment of anticipatory activity to various durations of food access. Physio & Behav. 1989; 46:731–741.

35. Verwey M, Amir S. Nucleus-specific effects of meal duration on daily profiles of Period1 and Period2 protein expression in rats housed under restricted feeding. Neuroscience. 2011; 192:304–311. pmid:21767615

36. Hoane MR, Irish SL, Marks BB, Barth TM. Preoperative regimens of magnesium facilitate recovery of function and prevent subcortical atrophy following lesions of the rat sensorimotor cortex. Brain Res Bulletin. 1998; 45:45–51.

37. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000; 404:661–671. pmid:10766253

38. Berridge KC, Robinson TE. Parsing reward. Trends in Neuroscience. 2003; 26:507–513.

39. Pomonis JD, Levine AS, Billington CJ. Interaction of the hypothalamic paraventricular nucleus and central nucleus of the amygdala in naloxone blockade of neuropeptide Y-induced feeding revealed by c-fos expression. J Neurosci. 1997; 17:5175–5182. pmid:9185555

40. Wang G-J, Volkow ND, Telang F, Jayne M, Ma J, et al. Exposure to appetitive food stimuli markedly activates the human brain. NeuroImage. 2004; 21:1790–1797. pmid:15050599

41. Mendoza J, Angeles-Castellanos M, Escobar C. Differential role of the accumbens shell and core subterritories in food-entrained rhythms of rats. Behav Brain Res. 2005; 158:133–142. pmid:15680201

42. Mistlberger RE, Rusak B. Palatable daily meals entrain anticipatory activity rhythms in free-feeding rats: dependence on meal size and nutrient content. Physiol & Behav. 1987; 41:219–226.
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