Rhythmic neuronal activities of the rat nucleus of the solitary tract are impaired by high-fat diet - implications for daily control of satiety.
circadian clock
food intake
high-fat diet
multi-electrode arrays
nucleus of the solitary tract
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
27
04
2021
accepted:
18
08
2021
pubmed:
8
9
2021
medline:
22
2
2022
entrez:
7
9
2021
Statut:
ppublish
Résumé
Temporal partitioning of daily food intake is crucial for survival and involves the integration of internal circadian states and external influences such as the light-dark cycle and dietary composition. These intrinsic and extrinsic factors are interdependent with misalignment of circadian rhythms promoting body weight gain, while consumption of a calorie-dense diet elevates the risk of obesity and blunts circadian rhythms. Recently, we defined the circadian properties of the dorsal vagal complex of the brainstem, a structure implicated in the control of food intake and autonomic tone, but whether and how 24 h rhythms in this area are influenced by diet remains unresolved. Here we focused on a key structure of this complex, the nucleus of the solitary tract (NTS). We used a combination of immunohistochemical and electrophysiological approaches together with daily monitoring of body weight and food intake to interrogate how the neuronal rhythms of the NTS are affected by a high-fat diet. We report that short-term consumption of a high-fat diet increases food intake during the day and blunts NTS daily rhythms in neuronal discharge. Additionally, we found that a high-fat diet dampens NTS responsiveness to metabolic neuropeptides, and decreases orexin immunoreactive fibres in this structure. These alterations occur without prominent body weight gain, suggesting that a high-fat diet acts initially to reduce activity in the NTS to disinhibit mechanisms that suppress daytime feeding. KEY POINTS: The dorsal vagal complex of the rodent hindbrain possesses intrinsic circadian timekeeping mechanisms In particular, the nucleus of the solitary tract (NTS) is a robust circadian oscillator, independent of the master suprachiasmatic clock Here, we reveal that rat NTS neurons display timed daily rhythms in their neuronal activity and responsiveness to ingestive cues These daily rhythms are blunted or eliminated by a short-term high-fat diet, together with increased consumption of calories during the behaviourally quiescent day Our results help us better understand the circadian control of satiety by the brainstem and its malfunctioning under a high-fat diet.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
751-767Informations de copyright
© 2021 The Authors. The Journal of Physiology © 2021 The Physiological Society.
Références
Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, Sakaki Y, Menaker M & Block GD (2002). Circadian rhythms in isolated brain regions. J Neurosci 22, 350-356.
Acuna-Goycolea C & van den Pol AN (2004). Glucagon-like peptide 1 excites hypocretin/orexin neurons by direct and indirect mechanisms: implications for viscera-mediated arousal. J Neurosci 24, 8141-8152.
Azeez IA, Del Gallo F, Cristino L & Bentivoglio M (2018). Daily fluctuation of orexin neuron activity and wiring: the challenge of “chronoconnectivity.” Front. Pharmacol. 9, 1061.
Baron KG & Reid KJ (2014). Circadian misalignment and health. Int. Rev. Psychiatry 26, 139-154.
Begg DP & Woods SC (2013). The endocrinology of food intake. Nat Rev Endocrinol 9, 584-597.
Belle MDC, Baño-Otalora B & Piggins HD (2021). Perforated multi-electrode array recording in hypothalamic brain slices. In Methods in molecular biology (Clifton, N.J), pp. 263-285.
Challet E (2015). Keeping circadian time with hormones. Diabetes, Obesity and Metabolism 17, 76-83.
Challet E (2019). The circadian regulation of food intake. Nat Rev Endocrinol 15, 393-405.
Chrobok L, Klich JD, Jeczmien-Lazur JS, Pradel K, Palus-Chramiec K, Sanetra AM, Piggins HD & Lewandowski MH (2021a). Daily changes in neuronal activities of the dorsal motor nucleus of the vagus under standard and high-fat diet. J Physiol, JP281596.
Chrobok L, Northeast RC, Myung J, Cunningham PS, Petit C & Piggins HD (2020). Timekeeping in the hindbrain: a multi-oscillatory circadian centre in the mouse dorsal vagal complex. Commun. Biol. 3, 1-12.
Chrobok L, Wojcik M, Klich JD, Pradel K, Lewandowski MH & Piggins HD (2021b). Phasic neuronal firing in the rodent nucleus of the solitary tract ex vivo. Front. Physiol. 12, 638695.
Crespo CS, Cachero AP, Jiménez LP, Barrios V & Ferreiro EA (2014). Peptides and food intake. Front. Endocrinol. 5, 1-13.
Cutler DJ, Morris R, Sheridhar V, Wattam TAK, Holmes S, Patel S, Arch JRS, Wilson S, Buckingham RE, Evans ML, Leslie RA & Williams G (1999). Differential distribution of orexin-A and orexin-B immunoreactivity in the rat brain and spinal cord. Peptides 20, 1455-1470.
Engin A (2017). Circadian rhythms in diet-induced obesity. In Advances in Experimental Medicine and Biology, pp. 19-52.
Fortin SM, Lipsky RK, Lhamo R, Chen J, Kim E, Borner T, Schmidt HD & Hayes MR (2020). GABA neurons in the nucleus tractus solitarius express GLP-1 receptors and mediate anorectic effects of liraglutide in rats. Sci Transl Med 12, eaay8071.
Funato H, Tsai AL, Willie JT, Kisanuki Y, Williams SC, Sakurai T & Yanagisawa M (2009). Enhanced orexin receptor-2 signaling prevents diet-induced obesity and improves leptin sensitivity. Cell Metab 9, 64-76.
Furnes MW, Zhao C-M & Chen D (2009). Development of obesity is associated with increased calories per meal rather than per day. A study of high-fat diet-induced obesity in young rats. Obes Surg 19, 1430-1438.
Gil-Lozano M, Mingomataj EL, Wu WK, Ridout SA & Brubaker PL (2014). Circadian Secretion of the Intestinal Hormone GLP-1 by the Rodent L Cell. Diabetes 63, 3674-3685.
Gil-Lozano M, Wu WK, Martchenko A & Brubaker PL (2016). High-fat diet and palmitate alter the rhythmic secretion of glucagon-like peptide-1 by the rodent L-cell. Endocrinology 157, 586-599.
Gonnissen HKJ, Hulshof T & Westerterp-Plantenga MS (2013). Chronobiology, endocrinology, and energy- and food-reward homeostasis. Obes Rev 14, 405-416.
Grill HJ & Hayes MR (2012). Hindbrain neurons as an essential hub in the neuroanatomically distributed control of energy balance. Cell Metab 16, 296-309.
Grundy D (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. J Physiol 593, 2547-2549.
Guilding C, Hughes ATL, Brown TM, Namvar S & Piggins HD (2009). A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Molecular brain 2, 28.
Guilding C & Piggins HD (2007). Challenging the omnipotence of the suprachiasmatic timekeeper: Are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25, 3195-3216.
Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, Sugiyama F, Yagami K, Goto K, Yanagisawa M & Sakurai T (2001). Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 30, 345-354.
Hariri N & Thibault L (2010). High-fat diet-induced obesity in animal models. Nutr Res Rev 23, 270-299.
Hastings MH, Maywood ES & Brancaccio M (2018). Generation of circadian rhythms in the suprachiasmatic nucleus. Nat Rev Neurosci 19, 453-469.
Herichová I, Mravec B, Stebelová K, Križanová O, Jurkovičová D, Kvetňanský R & Zeman M (2007). Rhythmic clock gene expression in heart, kidney and some brain nuclei involved in blood pressure control in hypertensive TGR(mREN-2)27 rats. Mol Cell Biochem 296, 25-34.
Kaneko K, Yamada T, Tsukita S, Takahashi K, Ishigaki Y, Oka Y & Katagiri H (2009). Obesity alters circadian expressions of molecular clock genes in the brainstem. Brain Res 1263, 58-68.
Kentish SJ, Christie S, Vincent A, Li H, Wittert GA & Page AJ (2019). Disruption of the light cycle ablates diurnal rhythms in gastric vagal afferent mechanosensitivity. Neurogastroenterol. Motil. 31, e13711. https://doi.org/10.1111/nmo.13711.
Kentish SJ, Vincent AD, Kennaway DJ, Wittert GA & Page AJ (2016). High-fat diet-induced obesity ablates gastric vagal afferent circadian rhythms. J Neurosci 36, 3199-3207.
Kohsaka A, Laposky AD, Ramsey KM, Estrada C, Joshu C, Kobayashi Y, Turek FW & Bass J (2007). High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 6, 414-421.
Kotz C, Nixon J, Butterick T, Perez-Leighton C, Teske J & Billington C (2012). Brain orexin promotes obesity resistance. Ann N Y Acad Sci 1264, 72-86.
Li S-B & de Lecea L (2020). The hypocretin (orexin) system: from a neural circuitry perspective. Neuropharmacology 167, 107993.
Linehan V, Fang LZ & Hirasawa M (2018). Short-term high-fat diet primes excitatory synapses for long-term depression in orexin neurons. J Physiol 596, 305-316. https://doi.org/10.1113/JP275177.
Marston OJ, Williams RH, Canal MM, Samuels RE, Upton N & Piggins HD (2008). Circadian and dark-pulse activation of orexin/hypocretin neurons. Molecular brain 1, 19.
Mistlberger RE (2011). Neurobiology of food anticipatory circadian rhythms. Physiol Behav 104, 535-545.
Mistlberger RE & Antle MC (2011). Entrainment of circadian clocks in mammals by arousal and food. Essays Biochem 49, 119-136.
Nobunaga M, Obukuro K, Kurauchi Y, Hisatsune A, Seki T, Tsutsui M & Katsuki H (2014). High fat diet induces specific pathological changes in hypothalamic orexin neurons in mice. Neurochem Int 78, 61-66.
Northeast RC, Chrobok L, Hughes ATL, Petit C & Piggins HD (2020a). Keeping time in the lamina terminalis: novel oscillator properties of forebrain sensory circumventricular organs. FASEB J 34, 974-987.
Northeast RC, Vyazovskiy V V. & Bechtold DA (2020b). Eat, sleep, repeat: the role of the circadian system in balancing sleep-wake control with metabolic need. Curr. Opin. Physiol. 15, 183-191.
Pachitariu M, Steinmetz N, Kadir S, Carandini M & Harris KD (2016). Kilosort: realtime spike-sorting for extracellular electrophysiology with hundreds of channels. bioRxiv; https://doi.org/10.1101/061481.
Paul JR, Davis JA, Goode LK, Becker BK, Fusilier A, Meador-Woodruff A & Gamble KL (2020). Circadian regulation of membrane physiology in neural oscillators throughout the brain. Eur J Neurosci 51, 109-138.
Pendergast JS, Branecky KL, Yang W, Ellacott KLJ, Niswender KD & Yamazaki S (2013). High-fat diet acutely affects circadian organisation and eating behavior. Eur J Neurosci 37, 1350-1356.
Peyron C, Tighe DK, van den Pol a N, de Lecea L, Heller HC, Sutcliffe JG & Kilduff TS (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18, 9996-10015.
Richard JE, Anderberg RH, Göteson A, Gribble FM, Reimann F & Skibicka KP (2015). Activation of the GLP-1 Receptors in the nucleus of the solitary tract reduces food reward behavior and targets the mesolimbic system ed. Chowen JA. PLoS One 10, e0119034.
Sabbatini M, Molinari C, Grossini E, Mary DASG, Vacca G & Cannas M (2004). The pattern of c-Fos immunoreactivity in the hindbrain of the rat following stomach distension. Exp Brain Res 157, 315-323.
Sakhi K, Wegner S, Belle MDC, Howarth M, Delagrange P, Brown TM & Piggins HD (2014). Intrinsic and extrinsic cues regulate the daily profile of mouse lateral habenula neuronal activity. J Physiol 592, 5025-5045.
Takahashi JS (2017). Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet 18, 164-179.
Velloso LA & Schwartz MW (2011). Altered hypothalamic function in diet-induced obesity. Int J Obes 35, 1455-1465.
Verwey M & Amir S (2009). Food-entrainable circadian oscillators in the brain. Eur J Neurosci 30, 1650-1657.
Vettor R, Fabris R, Pagano C & Federspil G (2002). Neuroendocrine regulation of eating behavior. J Endocrinol Invest 25, 836-854.
Yamanaka A, Sakurai T, Katsumoto T, Yanagisawa M & Goto K (1999). Chronic intracerebroventricular administration of orexin-A to rats increases food intake in daytime, but has no effect on body weight. Brain Res 849, 248-252.
Yang B & Ferguson AV (2003). Orexin-A depolarizes nucleus tractus solitarius neurons through effects on nonselective cationic and K+ conductances. J Neurophysiol 89, 2167-2175.
Yang B, Samson WK & Ferguson A V (2003). Excitatory effects of orexin-A on nucleus tractus solitarius neurons are mediated by phospholipase C and protein kinase C. J Neurosci 23, 6215-6222.
Zarrinpar A, Chaix A & Panda S (2016). Daily eating patterns and their impact on health and disease. Trends Endocrinol. Metab. 27, 69-83.
Zhang C, Barkholt P, Nielsen JC, Thorbek DD, Rigbolt K, Vrang N, Woldbye DPD & Jelsing J (2020). The dorsomedial hypothalamus and nucleus of the solitary tract as key regulators in a rat model of chronic obesity. Brain Res 1727, 146538.