in

Coprophagy prevention alters microbiome, metabolism, neurochemistry, and cognitive behavior in a small mammal

  • 1.

    Sommer F, Backhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol. 2013;11:227–38.

    CAS  PubMed  Google Scholar 

  • 2.

    Heijtz RD, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA. 2011;108:3047–52.

    CAS  Google Scholar 

  • 3.

    Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S. Gut microbial communities modulating brain development and function. Gut Microbes. 2012;3:366–73.

    PubMed  PubMed Central  Google Scholar 

  • 4.

    Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325–40.

    Google Scholar 

  • 5.

    Mackie RI. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integr Comp Biol. 2002;42:319–26.

    PubMed  Google Scholar 

  • 6.

    Bergman EJ. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70:567–90.

    CAS  PubMed  Google Scholar 

  • 7.

    Justice KE, Smith FA. A model of dietary fiber utilization by small mammalian herbivores, with empirical results for Neotoma. Am Naturalist. 1992;139:398–416.

    Google Scholar 

  • 8.

    Stevens CE, Hume ID. Comparative physiology of the vertebrate digestive system. Cambridge University Press; UK, 2004.

  • 9.

    Matsuzawa T, Nakata M, Tsushima M. Feeding and excretion in the Afghan pika (Ochotona rufescens rufescens), a new laboratory animal. Lab Anim. 1981;15:319–22.

    CAS  PubMed  Google Scholar 

  • 10.

    Liu QS, Wang DH. Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus). J Comp Physiol B. 2007;177:509–18.

    CAS  PubMed  Google Scholar 

  • 11.

    Pei YX, Wang DH, Hume ID. Selective digesta retention and coprophagy in Brandt’s vole (Microtus brandti). J Comp Physiol B. 2001;171:457–64.

    CAS  PubMed  Google Scholar 

  • 12.

    Savage DC. Gastrointestinal microflora in mammalian nutrition. Annu Rev Nutr. 1986;6:155–78.

    CAS  PubMed  Google Scholar 

  • 13.

    Klaasen HLBM, Koopman JP, Scholten PM, Van DBME, Theeuwes AGM. Effect of preventing coprophagy on colonisation by segmented filamentous bacteria in the small bowel of mice. Microb Ecol Health Dis. 1990;3:99–103.

    Google Scholar 

  • 14.

    Fitzgerald RJ, Gustafsson BE, McDaniel EG. Effects of coprophagy prevention on intestinal microflora in rats. J Nutr. 1964;84:155–60.

    CAS  PubMed  Google Scholar 

  • 15.

    Sarkar A, Harty S, Lehto SM, Moeller AH, Dinan TG, Dunbar RIM, et al. The microbiome in psychology and cognitive neuroscience. Trends Cogn Sci. 2018;22:611–36.

    PubMed  Google Scholar 

  • 16.

    Sandhu KV, Eoin Sherwin HS, Catherine S, Timothy GD, John FC. Feeding the microbiota-gut-brain axis: diet, microbiome, and neuropsychiatry. Transl Res. 2017;179:223–44.

    CAS  PubMed  Google Scholar 

  • 17.

    Ling Z, Cheng Y, Li L. Gut microbiota depletion from early adolescence in mice: Implications for brain and behavior. Brain Behav Immun. 2015;48:165–73.

    Google Scholar 

  • 18.

    Sampson TR, Mazmanian SK. Control of brain development, function, and behavior by the microbiome. Cell Host Microbe. 2015;17:565–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 19.

    Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458–62.

    CAS  PubMed  Google Scholar 

  • 20.

    Wang X, Wang BR, Zhang XJ, Xu Z, Ding YQ, Ju G. Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats. World J Gastroenterol. 2002;8:540–5.

    PubMed  PubMed Central  Google Scholar 

  • 21.

    Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA. 2011;108:16050–5.

    CAS  PubMed  Google Scholar 

  • 22.

    Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242–9.

    CAS  PubMed  Google Scholar 

  • 23.

    Ziętak M, Kovatcheva-Datchary P, Markiewicz LH, Ståhlman M, Kozak LP, Bäckhed F. Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab. 2016;23:1216–23.

    PubMed  PubMed Central  Google Scholar 

  • 24.

    Bo TB, Zhang XY, Wen J, Deng K, Qin XW, Wang DH. The microbiota-gut-brain interaction in regulating host metabolic adaptation to cold in male Brandt’s voles (Lasiopodomys brandtii). ISME J. 2019;13:3037–53.

    CAS  PubMed  Google Scholar 

  • 25.

    Laukens D, Brinkman BM, Raes J, De Vos M, Vandenabeele P. Heterogeneity of the gut microbiome in mice: guidelines for optimizing experimental design. FEMS Microbiol Rev. 2016;40:117–32.

    CAS  PubMed  Google Scholar 

  • 26.

    Haim A, Izhaki I. The ecological significance of resting metabolic rate and non-shivering thermogenesis for rodents. J Therm Biol. 1993;18:71–81.

    Google Scholar 

  • 27.

    Burton T, Killen SS, Armstrong JD, Metcalfe NB. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?. Proc R Soc B: Biol Sci. 2011;278:3465–73.

    CAS  Google Scholar 

  • 28.

    Zhang XY, Sukhchuluun G, Bo TB, Chi QS, Yang JJ, Wang DH, et al. Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome. 2018;6:103.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 29.

    Montiglio PO, Garant D, Thomas D, Reale D. Individual variation in temporal activity patterns in open-field tests. Anim Behav. 2010;80:905–12.

    Google Scholar 

  • 30.

    Yao W, Liu W, Deng K, Wang Z, Wang DH, Zhang XY. GnRH expression and cell proliferation are associated with seasonal breeding and food hoarding in Mongolian gerbils (Meriones unguiculatus). Horm Behav. 2019;112:42–53.

    CAS  PubMed  Google Scholar 

  • 31.

    Lieberwirth C, Liu Y, Jia X, Wang Z. Social isolation impairs adult neurogenesis in the limbic system and alters behaviors in female prairie voles. Horm Behav. 2012;62:357–66.

    PubMed  PubMed Central  Google Scholar 

  • 32.

    Cardiff RD, Miller CH, Munn RJ. Manual hematoxylin and eosin staining of mouse tissue sections. Cold Spring Harb Protoc. 2014;6:073411.

    Google Scholar 

  • 33.

    Rueden CT, Schindelin JE, Hiner MC, DeZonia BE, Walter AE, Arena ET, et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinform. 2017;18:529.

    Google Scholar 

  • 34.

    Chiu K, Lau WM, Lau HT, So KF, Chang RCC. Micro-dissection of rat brain for RNA or protein extraction from specific brain region. J Vis Exp. 2017;7:269.

  • 35.

    Jia M, Meng F, Smerin SE, Xing G, Zhang L, Su DM, et al. Biomarkers in an animal model for revealing neural, hematologic, and behavioral correlates of PTSD. J Vis Exp. 2012;68:3361.

  • 36.

    Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011;5:1571–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 37.

    Douglas GM, Maffei VJ, Zaneveld J R, Yurgel SN, Langille MGI.  PICRUSt2 for prediction of metagenome functions. Nature Biotechnology. 2020; D1:1-5.

  • 38.

    Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 39.

    Cartmell J, Salhoff CR, Perry KW, Monn JA, Schoepp DD. Dopamine and 5-HT turnover are increased by the mGlu2/3 receptor agonist LY379268 in rat medial prefrontal cortex, nucleus accumbens and striatum. Brain Res. 2000;887:378–84.

    CAS  PubMed  Google Scholar 

  • 40.

    Kim KI, van de Wiel MA. Effects of dependence in high-dimensional multiple testing problems. BMC Bioinform. 2008;9:114.

    Google Scholar 

  • 41.

    Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Huttenhower C, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.

    PubMed  PubMed Central  Google Scholar 

  • 42.

    Hörnicke H, Björnhag G. Coprophagy and related strategies for digesta utilization. In: Ruckebusch Y., Thivend P. (eds) Digestive physiology and metabolism in ruminants. Published by MTP Press Limited, England, 1980;34:707–30.

  • 43.

    Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Gordon JI, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101:15718–23.

    PubMed  Google Scholar 

  • 44.

    Li H, Qu J, Li T, Wirth S, Zhang Y, Li X, et al. Diet simplification selects for high gut microbial diversity and strong fermenting ability in high-altitude pikas. Appl Microbiol Biotechnol. 2018;102:6739–51.

    CAS  PubMed  Google Scholar 

  • 45.

    Sommer F, StHlman M, Ilkayeva O, Arnemo J, Kindberg J, Josefsson J, et al. The Gut Microbiota Modulates Energy Metabolism in the hibernating brown bear Ursus arctos. Cell Rep. 2016;14:1655–61.

    CAS  PubMed  Google Scholar 

  • 46.

    Klaasen HL, Koopman JP, Poelma FG, Beynen AC. Intestinal, segmented, filamentous bacteria. FEMS Microbiol Rev. 1992;8:165–79.

    CAS  PubMed  Google Scholar 

  • 47.

    Sagheddu V, Patrone V, Miragoli F, Puglisi E, Morelli L. Infant early gut colonization by Lachnospiraceae: high frequency of Ruminococcus gnavus. Front Pediatr. 2016;4:57.

    PubMed  PubMed Central  Google Scholar 

  • 48.

    Præsteng KE, Pope PB, Cann IKO, Mackie RI, Mathiesen SD, Sundset MA, et al. Probiotic dosing of Ruminococcus flavefaciens affects rumen microbiome structure and function in reindeer. Micro Ecol. 2013;66:840–9.

    Google Scholar 

  • 49.

    Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, Zoetendal EG, et al. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 2013;7:707–17.

    CAS  PubMed  Google Scholar 

  • 50.

    Goodrich J, DiRienzi S, Poole A, Koren O, Walters W, Caporaso J, et al. Conducting a microbiome study. Cell. 2014;158:250–62.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 51.

    Verdam FJ, Fuentes S, de Jonge C, Zoetendal EG, Erbil R, Rensen SS, et al. Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity. 2013;21:E607–15.

    CAS  PubMed  Google Scholar 

  • 52.

    David LA, Maurice C, Carmody RN, Gootenberg DB, Button JE, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63.

    CAS  Google Scholar 

  • 53.

    Kohl KD, Miller AW, Marvin JE, Mackie R, Dearing MD. Herbivorous rodents (Neotoma spp.) harbour abundant and active foregut microbiota. Environ Microbiol. 2014;16:2869–78.

    CAS  PubMed  Google Scholar 

  • 54.

    Carmody RN, Gerber GK, Luevano JM, Gatti DM, Somes L, Turnbaugh PJ, et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe. 2015;17:72–84.

    CAS  PubMed  Google Scholar 

  • 55.

    Liu QS, Li JY, Wang DH. Ultradian rhythms and the nutritional importance of caecotrophy in captive Brandt’s voles (Lasiopodomys brandtii). J Comp Physiol B. 2007;177:423–32.

    PubMed  Google Scholar 

  • 56.

    Zhang C, Li S, Yang L, Huang P, Li W, Zhao L, et al. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat Commun. 2013;4:2163.

    PubMed  PubMed Central  Google Scholar 

  • 57.

    Cree TC, Wadley DM, Marlett JA. Effect of preventing coprophagy in the rat on neutral detergent fiber digestibility and apparent calcium absorption. J Nutr. 1986;116:1204–8.

    CAS  PubMed  Google Scholar 

  • 58.

    Sukemori S, Ikeda S, Kurihara Y, Ito S. Amino acid, mineral and vitamin levels in hydrous faeces obtained from coprophagy-prevented rats. J Anim Physiol Anim Nutr. 2003;87:213–20.

    CAS  Google Scholar 

  • 59.

    Cranford JA, Johnson EO. Effects of coprophagy and diet quality on two microtine rodents (Microtus pennsylvanicus and Microtus pinetorum). J Mammal. 1989;70:494–502.

    Google Scholar 

  • 60.

    Stillings BR, Hackler LR. Effect of coprophagy on protein utilization in the rat. J Nutr. 1966;90:19–24.

    CAS  PubMed  Google Scholar 

  • 61.

    Dunel-Erb S, Chevalier C, Laurent P, Bach A, Decrock F, Le Maho Y. Restoration of the jejunal mucosa in rats refed after prolonged fasting. Comp Biochem Physiol Part A: Mol Integr Physiol. 2001;129:933–47.

    CAS  Google Scholar 

  • 62.

    Merry BJ. Molecular mechanisms linking calorie restriction and longevity. Int J Biochem Cell Biol. 2002;34:1340–54.

    CAS  PubMed  Google Scholar 

  • 63.

    Sauberlich HJ. Amino acid imbalance as related to methionine, isoleucine, threonine and tryptophan requirement of the rat or mouse. J Nutr. 1956;59:353–70.

    CAS  PubMed  Google Scholar 

  • 64.

    Yan L, Sun X, Wang Z, Song M, Zhang Z. Regulation of social behaviors by p-Stat3 via oxytocin and its receptor in the nucleus accumbens of male Brandt’s voles (Lasiopodomys brandtii). Horm Behav. 2020;119:104638.

    CAS  PubMed  Google Scholar 

  • 65.

    Janson CH. Experimental evidence for spatial memory in foraging wild capuchin monkeys, Cebus apella. Anim Behav. 1998;55:1229–43.

    CAS  PubMed  Google Scholar 

  • 66.

    Phelps SM, Rand AS, Ryan MJ. A cognitive framework for mate choice and species recognition. Am Naturalist. 2006;167:28–42.

    Google Scholar 

  • 67.

    Parker JT, Rodriguez N, Lawal B, Delevan CJ, & Bamshad M. Mating increases male’s interest in other females: a cognitive study in socially monogamous prairie voles (microtus ochrogaster). Behav Processes. 2011;88:127–34.

    PubMed  Google Scholar 

  • 68.

    Burkart JM, Van Schaik CP. Cognitive consequences of cooperative breeding in primates?. Anim Cognition. 2010;13:1–19.

    Google Scholar 

  • 69.

    Luine V, Hearns M. Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res. 1990;523:321–4.

    CAS  PubMed  Google Scholar 

  • 70.

    Bowman RE, Beck KD, Luine VN. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Hormones Behav. 2003;43:48–59.

    CAS  Google Scholar 

  • 71.

    Deng XH, Liu Y, Chen ZG. Memory-based evolutionary game on small-world network with tunable heterogeneity. Phys A: Stat Mech its Appl. 2010;389:5173–81.

    Google Scholar 

  • 72.

    Malberg JE, Eisch AJ, Nestler EJ, Duman RS. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci. 2000;20:9104–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 73.

    Vadder FD, Grasset E, Holm LM, Karsenty G, Macpherson AJ, Bäckhed F, et al. Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks. Proc Natl Acad Sci USA. 2018;115:6458–63.

    CAS  PubMed  Google Scholar 

  • 74.

    O’Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. 2015;277:32–48.

    PubMed  Google Scholar 

  • 75.

    Liebsch G, Wotjak CT, Landgraf R, Engelmann M. Septal vasopressin modulates anxiety-related behavior in rats. Neurosci Lett. 1996;217:101–4.

    CAS  PubMed  Google Scholar 

  • 76.

    Cilz NI, Cymerblit-Sabba A, Young WS. Oxytocin and vasopressin in the rodent hippocampus. Genes Brain Behav. 2019;18:e12535.

    PubMed  Google Scholar 

  • 77.

    Johnson ZV, Young LJ. Oxytocin and vasopressin neural networks: Implications for social behavioral diversity and translational neuroscience. Neurosci Biobehav Rev. 2017;76:87–98.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 78.

    Hamburger-Bar, Klein R,A, Belmaker RH. The effect of chronic vs. acute injection of vasopressin on animal learning and memory. Peptides. 1985;6:23–5.

    CAS  PubMed  Google Scholar 

  • 79.

    Bluthe RM, Koob GF, Dantzer R. Hypertonic saline mimics the effects of vasopressin and social recognition in rats. Behav Pharm. 1991;2:513–6.

    Google Scholar 

  • 80.

    Bohus B, Urban I, Vanwimersmagreidanus T, Dewied D. Opposite effects of oxytocin and vasopressin on avoidance behavior and hippocampal theta rhythm in the rat. Neuropharmacology. 1978;17:239–47.

    CAS  PubMed  Google Scholar 

  • 81.

    Metzger D, Alescio-Lautier B, Bosler O, Devigne C, Soumireu-Mourat B. Effect of changes in the intrahippocampal vasopressin on memory retrieval and relearning. Behav Neural Biol. 1993;59:29–48.

    CAS  PubMed  Google Scholar 

  • 82.

    Dietrich A, Allen JD. Vasopressin and memory. II. Lesions to the hippocampus block the memory enhancing effects of AVP4-9 in the radial maze. Behav Brain Res. 1997;87:201–8.

    CAS  PubMed  Google Scholar 

  • 83.

    Yang C, Zhang X, Gao J, Wang M, Yang Z. Arginine vasopressin ameliorates spatial learning impairments in chronic cerebral hypoperfusion via V1a receptor and autophagy signaling partially. Transl Psychiatry. 2017;7:e1174.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 84.

    Popik P, Van Ree JM. Long-term facilitation of social recognition in rats by vasopressin related peptides: a structure-activity study. Life Sci. 1992;50:567–72.

    CAS  PubMed  Google Scholar 

  • 85.

    Lee SY, Park SH, Chung C, Kim JJ, Choi SY, Han JS. Oxytocin protects hippocampal memory and plasticity from uncontrollable stress. Sci Rep. 2015;5:18540.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 86.

    Burkett JP, Andari E, Johnson ZV, Curry DC, de Waal FBM, Young LJ. Oxytocin-dependent consolation behavior in rodents. Science. 2016;351:375–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 87.

    Gobrogge KL, Jia X, Liu Y, Wang Z. Neurochemical mediation of affiliation and aggression associated with pair-bonding. Biol Psychiatry. 2017;81:231–42.

    CAS  PubMed  Google Scholar 

  • 88.

    Freeman AR, Hare JF, Anderson WG, Caldwell HK. Effects of arginine vasopressin on Richardson’s ground squirrel social and vocal behavior. Behav Neurosci. 2018;132:34.

    PubMed  Google Scholar 

  • 89.

    Kohl KD, Carey HV. A place for host–microbe symbiosis in the comparative physiologist’s toolbox. J Exp Biol. 2016;219:3496–504.

    PubMed  Google Scholar 

  • 90.

    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.

    PubMed  PubMed Central  Google Scholar 

  • 91.

    Stilling RM, Dinan TG, Cryan JF. Microbial genes, brain & behavior—epigenetic regulation of the gut-brain axis. Genes Brain Behav. 2014;13:69–86.

    CAS  PubMed  Google Scholar 

  • 92.

    Luczynski P, Whelan SO, O’Sullivan C, Clarke G, Shanahan F, Dinan TG, et al. Adult microbiota-deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus. Eur J Neurosci. 2016;44:2654–66.

    PubMed  PubMed Central  Google Scholar 

  • 93.

    Zambell KL, Fitch MD, Fleming SE. Acetate and butyrate are the major substrates for de novo lipogenesis in rat colonic epithelial cells. J Nutr. 2003;133:3509–15.

    CAS  PubMed  Google Scholar 

  • 94.

    Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13:517–26.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 95.

    Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004;91:915–23.

    CAS  PubMed  Google Scholar 

  • 96.

    Harada E, Kato S. Effect of short-chain fatty acids on the secretory response of the ovine exocrine pancreas. Am J Physiol. 1983;244:G284–90.

    CAS  PubMed  Google Scholar 

  • 97.

    Kvietys PR, Granger DN. Effect of volatile fatty acids on blood flow and oxygen uptake by the dog colon. Gastroenterology. 1981;80:962–9.

    CAS  PubMed  Google Scholar 

  • 98.

    Whittle N, Singewald N. HDAC inhibitors as cognitive enhancers in fear, anxiety and trauma therapy: where do we stand?. Biochemical Soc Trans. 2014;42:569.

    CAS  Google Scholar 

  • 99.

    Singewald N, Schmuckermair C, Whittle N, Holmes A, Ressler KJ. Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders. Pharm Ther. 2015;149:150–90.

    CAS  Google Scholar 

  • 100.

    Van de Wouw M, Boehme M, Lyte JM, Wiley N, Strain C, Cryan JF, et al. Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain-gut axis alterations. J Physiol. 2018;596:4923–44.

    PubMed  PubMed Central  Google Scholar 

  • 101.

    Kaptan Z, Akgün-Dar K, Kapucu A, Dedeakayoğulları H, Batu Ş, Üzüm G. Long term consequences on spatial learning-memory of low-calorie diet during adolescence in female rats; hippocampal and prefrontal cortex BDNF level, expression of NeuN and cell proliferation in dentate gyrus. Brain Res. 2015;1618:194–204.

    CAS  PubMed  Google Scholar 

  • 102.

    Engelmann M, Wotjak CT, Neumann I, Ludwig M, Landgraf R. Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory. Neurosci Biobehav Rev. 1996;20:341–58.

    CAS  PubMed  Google Scholar 

  • 103.

    Song Z, Larkin TE, Malley MO, Albers HE. Oxytocin (OT) and arginine-vasopressin (AVP) act on OT receptors and not AVP V1a receptors to enhance social recognition in adult Syrian hamsters (Mesocricetus auratus). Hormones Behav. 2016;81:20–27.

    CAS  Google Scholar 

  • 104.

    Dantzer R, Koob GF, Bluthe RM, Le Moal M. Septal vasopressin modulates social memory in male rats. Brain Res. 1988;457:143–7.

    CAS  PubMed  Google Scholar 

  • 105.

    Lukas M, Toth I, Veenema AH, Neumann ID. Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology. 2013;38:916–26.

    CAS  PubMed  Google Scholar 

  • 106.

    Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Blümcke I, et al. NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem. 1996;44:1167–71.

    CAS  PubMed  Google Scholar 


  • Source: Ecology - nature.com

    Progressive nitrogen limitation across the Tibetan alpine permafrost region

    Behavioural responses of white sharks to specific baits during cage diving ecotourism