Effects of Sterculia Apetala Seed Oil on Anxiety-like Behavior and Neuronal Cells in the Hippocampus in Rats

Isidro Vargas-Moreno¹, Juan-Francisco Rodríguez-Landa², Héctor-Gabriel Acosta-Mesa³, Rafael Fernández-Demeneghi¹, Rosamaria Oliart-Ros⁴, Daniel Hernández Baltazar⁵ and Socorro Herrera-Meza^6,

¹Institute of Neuroethology (doctoral program in neuroethology), University of Veracruz, Xalapa, Mexico

²Institute of Neuroethology, University of Veracruz, Xalapa, Veracruz, Mexico

³Artificial Intelligence Research Institute, University of Veracruz, Xalapa, Veracruz, Mexico

⁴National Technological Institute of Mexico, Food Research and Development Unit, Veracruz, Veracruz, Mexico

⁵CONACyT-Institute of Neuroethology, University of Veracruz, Xalapa, Veracruz, Mexico

⁶Institute of Psychological Research, University of Veracruz, Xalapa, Veracruz Mexico

Cite this paper:
Isidro Vargas-Moreno, Juan-Francisco Rodríguez-Landa, Héctor-Gabriel Acosta-Mesa, Rafael Fernández-Demeneghi, Rosamaria Oliart-Ros, Daniel Hernández Baltazar and Socorro Herrera-Meza. Effects of Sterculia Apetala Seed Oil on Anxiety-like Behavior and Neuronal Cells in the Hippocampus in Rats. Journal of Food and Nutrition Research. 2023; 11(3):211-222. doi: 10.12691/jfnr-11-3-6

Abstract

The present study evaluated anxiety-like behavior and neuronal changes in the CA1, CA3, and dentate gyrus subregions of the hippocampus that were induced by chronic sterculic oil administration in Wistar rats. The study included two experiments. The first experiment evaluated doses-response curves of sterculic oil (low dose, 0.06 g; medium dose, 0.12 g; high dose, 0.24 g). The second experiment evaluated the effects of sterculic oil on the number of adult hippocampal neurons. For all experiments, we employed a behavioral test battery that included the elevated plus maze, locomotor activity test, and forced swim test. All sterculic oil doses produced anxiogenic-like effects, without significant changes in locomotor activity or behavior in the forced swim test. We observed a reduction of neurons in the hippocampus in rat groups that were exposed to behavioral tests compared with a test-free vehicle group. Sterculia apetala seed oil administration produced anxiogenic-like effects, with a smaller effect of the medium dose on neurons in the CA1 and dentate gyrus regions of the hippocampus.

Keywords:
anxiety behavior hippocampus neurons Sterculia apetala

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References:

[1]	FAO: Food and Agriculture Organization of the United Nations, “Seeds”, FAO, 2020. [Online] Available: https://www.fao.org/seeds/en/ [Accessed Oct. 10, 2022]
[2]	FAO: Food and Agriculture Organization of the United Nations, “Nature's nutritious seeds: 10 reasons why you should opt for pulses”, FAO, 2019. [Online] Available: https://www.fao.org/fao-stories/article/es/c/1176992/ [Accessed Jul.14, 2022]
[3]	Lascurain, M., López-Binnqüist, C., López, J.C. (2018) El árbol de cachichín (Oecopetalum mexicanum) una especie cultural clave de Veracruz, México. In: Silva-Rivera, E., Martínez-Valdés, V., Lascurain, M., Rodríguez-Luna, De la recolección a los agroecosistemas diversificados: soberanía alimentaria y conservación de la biodiversidad, 1st edition. Veracruz, México, 2018, 225-236.
[4]	Román-Cortés, N., García-Mateos, M.R., Castillo-González, A.M., Sahagún-Castellanos, J., Jiménez-Arellanes, A. “Componentes nutricionales y antioxidantes de dos especies de guaje (Leucaena spp.): un recurso ancestral subutilizado”, Revista Chapingo. Serie horticultura, 20(2). 157-170. August 2014.
[5]	Penington T.D., Sarukhan J. Descripción de especies. In: Penington T.D., Sarukhan, J. Árboles tropicales de México para la identificación de las principales especies, (2nd reprint of the 3rd edition), National Autonomous University of Mexico, México, 2016, 384-385.
[6]	Herrera-Meza, S., Martínez, A.J., Sánchez-Otero, M.G., Mendoza-López, M.R., García-Barradas, O., Ortiz-Viveros, G.R., Oliart-Ros, R.M. “Fatty acid composition and some physicochemical characteristics of Sterculia apetala seed oils”, Grasas y Aceites, 65(3). e039: 1-7. July–September 2014.
[7]	Bao, X., Thelen, J.J., Bonaventure, G., Ohlrogge, J.B. “Characterization of Cyclopropane Fatty-acid Synthase from Sterculia foetida”, The Journal Of Biological Chemistry, 278(15). 12846-12853. January, 2003.
[8]	Herrera-Meza, M.S., Mendoza-López, M.R., Garcıía-Barradas, O., Sanchez-Otero, M.G., Silva-Hernández, E.R., Angulo, J.O., Oliart-Ros, R.M. “Dietary anhydrous milk fat naturally enriched with conjugated linoleic acid and vaccenic acid modify cardiovascular risk biomarkers in spontaneously hypertensive rats”, International Journal of Food Sciences and Nutrition, 64(5). 574-586. January, 2013.
[9]	Ramírez-Higuera, A., Pena-Montes, C., Herrera-Meza, S., Mendoza-López, R., Valerio-Alfaro, G., Oliart-Ros, R.M. (2020) “Preventive Action of Sterculic Oil on Metabolic Syndrome Development on a Fructose-Induced Rat Model”, Journal of Medicinal Food, 23(3). 305-311. 2020.
[10]	Herrera-Meza, S., Rodríguez-Landa, J.F., Martínez, A.J., Herrera-Meza, G., Fernández-Demeneghi, R., Reyes-Saldana, K., Oliart-Ros, R.M. “Behavioral Effect of Sterculia apetala Seed Oil Consumption in Male Zucker Rats”, Journal of Medicinal Food, 20(11). 1133-1139. November 2017.
[11]	Rivadeneyra-Domínguez, E., Saavedra, M., Rodríguez-Landa, J.F. “El tratamiento con progesterona previene las alteraciones motoras inducidas por la intoxicación con semillas de cícada (Dioon spinulosum) en la rata macho”, Revista de Toxicología, 26(2-3). 117-121. April, 2009.
[12]	Carod-Artal, F.J. “Síndromes neurológicos asociados con el consumo de plantas y hongos con componente tóxico (I). Síndromes neurotóxicos por ingesta de plantas, semillas y frutos”, Revista de neurología (Ed. impresa), 36(9). 860-871. May 2003.
[13]	Saavedra, M., Rivadeneyra-Domínguez, E., Rodríguez-Landa, J.F. “Alteraciones motoras inducidas por la microinyección intrahipocampal de metilazoximetanol en ratas macho forzadas a nadar”, Archivos de Neurociencia (Méx), 16. 186-192. October-December 2011.
[14]	Rivadeneyra-Domínguez, E., Vazquez-Luna, A., Diaz-Sobac, R., Briones-Cespedes, E.E., Rodríguez-Landa, J.F. “Contribution of hippocampal area CA1 to acetone cyanohydrin-induced loss of motor coordination in rats”, Neurología (English Edition), 32(4). 230-235. 2017. May 2017.
[15]	Institute of Laboratory Animal Resources (US). Committee on Care, & Use of Laboratory Animals. Guide for the care and use of laboratory animals (No. 86). US Department of Health and Human Services, Public Health Service, National Institutes of Health, 1986.
[16]	NOM-062-ZOO-1999 Gobierno de México, “Norma Oficial Mexicana NOM-062-ZOO-1999, Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio”, México: Gobierno de México, 2001. [Online] Available: https://catalogonacional.gob.mx/FichaRegulacion?regulacionId=17652 [Accessed Jun. 22, 2022]
[17]	Johns Hopkins University, “The Principles of Humane Experimental Technique”, Johns Hopkins University, 2005. [Online] Available: https://caat.jhsph.edu/principles/the-principles-of-humane-experimental-technique [Accessed Sep. 22 2022].
[18]	Fernández-Demeneghi, R., Rodríguez-Landa, J.F., Guzmán-Gerónimo, R.I., Acosta-Mesa, H.G., Meza-Alvarado, E., Vargas-Moreno, I., & Herrera-Meza, S. “Effect of blackberry juice (Rubus fruticosus L.) on anxiety-like behaviour in Wistar rats”, International journal of food sciences and nutrition, 70(7). 856-867. January 2019.
[19]	Pellow, S., Chopin, P., File, S.E., Briley, M. “Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat”, Journal of Neuroscience Methods, 14(3). 149-167. August 1985.
[20]	Cohen, H., Matar, M.A., Joseph, Z. “Animal models of post-traumatic stress disorder”, Current Protocols in Neuroscience, 64(1). 9-45. July 2013.
[21]	Seibenhener, M.L., & Wooten, M.C. “Use of the open field maze to measure locomotor and anxiety-like behavior in mice”, Journal of visualized experiments, (96). e52434: 1-6. Febrary 2015.
[22]	Rodríguez-Landa, J.F., Cueto-Escobedo, J., Flores-Aguilar, L.Á., Rosas-Sánchez, G.U., Rovirosa-Hernández, M.J., García-Orduña, F., Carro-Juárez, M. “The Aqueous Crude Extracts of Montanoa frutescens and Montanoa grandiflora Reduce Immobility Faster Than Fluoxetine Through GABAA Receptors in Rats Forced to Swim”, Journal of Evidence-Based Integrative Medicine, 23. 1-12. Febrary 2018.
[23]	Contreras, C.M., Martínez-Mota, L., Saavedra, M. “Desipramine restricts estral cycle oscillations in swimming”, Progress in Neuro-Psychopharmacology and Biological Psychiatry, 2(7). 1121-1128. August 1998.
[24]	Borsini F. “Role of the serotonergic system in the forced swimming test”, Neuroscience & Biobehavioral Reviews, 19(3). 377–395. June 1995.
[25]	Rivadeneyra-Domínguez, E., Vázquez-Luna, A., Rodríguez-Landa, J.F., Díaz-Sobac, R. “A standardized extract of Ginkgo biloba prevents locomotion impairment induced by cassava juice in Wistar rats”, Frontiers in Pharmacology, 5(213). 1-6. September 2014.
[26]	Puga-Olguín, A., Rodríguez-Landa, J.F., Rovirosa-Hernández, M., Germán-Ponciano, L.J., Caba, M., Meza, E., Olmos-Vázquez, O.J. “Long-term ovariectomy increases anxiety-and despair-like behaviors associated with lower Fos immunoreactivity in the lateral septal nucleus in rats”, Behavioural Brain Research, 360. 185-195. March 2019.
[27]	Paxinos, G.A.W.C., Watson, C. The rat brain atlas in stereotaxic coordinates. San Diego, United States, 2014.
[28]	Zhu, Y., Liu, F., Zou, X., Torbey, M. “Comparison of unbiased estimation of neuronal number in the rat hippocampus with different staining methods”, Journal of Neuroscience Methods, 254. 73-79. October 2015.
[29]	Neira-Montoya, C., Sedano-Gelvet, E., Vilcarromero, V.M.E. Histología, Técnicas Microscópicas. Departamento Académico de Ciencias Morfológicas, Universidad Mayor de San Marcos, Lima, Perú. 2008.
[30]	Mitchell, T.M. Machine learning, McGraw-Hill Higher Education, United States. 1997.
[31]	Witten, I.H., Frank, E. “Data mining: practical machine learning tools and techniques with Java implementations”, Acm Sigmod Record, 31(1). 76-77. March 2002.
[32]	Tejada, J., Bosco, G.G., Morato, S., Roque, A.C. “Characterization of the rat exploratory behavior in the elevated plus-maze with Markov chains”, Journal of neuroscience methods, 193(2). 288-295. November 2010.
[33]	Vegetabile, B.G., Stout-Oswald, S.A., Davis, E.P., Baram, T.Z., Stern, H.S. “Estimating the entropy rate of finite Markov Chains with application to behavior studies”, Journal of Educational and Behavioral Statistics, 44(3). 282-308. November 2019.
[34]	Pellow, S., File, S.E. “Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat”, Pharmacology biochemistry and behavior, 24. 525-529. March 1986.
[35]	Bertagna, N.B., Dos Santos, P.G.C., Queiroz, R.M., Fernandes, G.J.D., Cruz, F.C., Miguel, T.T. “Involvement of the ventral, but not dorsal, hippocampus in anxiety-like behaviors in mice exposed to the elevated plus maze: participation of CRF1 receptor and PKA pathway”, Pharmacological Reports, 73(1). 57-72. Febrary 2021
[36]	Cohen, H., Zohar, J., Kaplan, Z., Arnt, J. “Adjunctive treatment with brexpiprazole and escitalopram reduces behavioral stress responses and increase hypothalamic NPY immunoreactivity in a rat model of PTSD-like symptoms”, European Neuropsychopharmacology, 28(1). 63-74. January 2018.
[37]	Sonavane, G.S., Sarveiya, V.P., Kasture, V.S., & Kasture, S.B. “Anxiogenic activity of Myristica fragrans seeds”, Pharmacology Biochemistry and Behavior, 71(1-2). 239-244. January–February 2002.
[38]	Kalueff, A.V., Tuohimaa, P. “The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research”, Journal of neuroscience methods, 143(2). 169-177. April 2005
[39]	Perrot-Sinal, T.S., Gregus, A., Boudreau, D., Kalynchuk, L.E. “Sex and repeated restraint stress interact to affect cat odor-induced defensive behavior in adult rats”, Brain research, 1027. 161-172. November 2004.
[40]	Detke, M.J., Rickels, M., Lucki, I. “Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants”, Psychopharmacology, 121(1). 66-72. September 1995.
[41]	Carobrez, A.P., Bertoglio, L.J. “Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on”, Neuroscience & Biobehavioral Reviews, 29. 1193–1205. August 2005.
[42]	Shishkina, G.T., Kalinina, T.S., Berezova, I.V., Bulygina, V.V., Dygalo, N.N. “Resistance to the development of stress-induced behavioral despair in the forced swim test associated with elevated hippocampal Bcl-xl expression”, Behavioural brain research, 213(2). 218-224. December 2010.
[43]	Sapolsky, R.M., Krey, L.C., McEwen, B.S. “The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis”, Science of Aging Knowledge Environment, 2002(38), cp21-cp21. September 2002.
[44]	Suvrathan, A., Tomar, A., Chattarji, S. “Effects of chronic and acute stress on rat behaviour in the forced-swim test”, Stress, 13(6). 533-540. July 2010.
[45]	Aisa, B., Tordera, R., Lasheras, B., Del Río, J., Ramírez, M.J. “Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats”, Psychoneuroendocrinology, 32(3). 256-266. April, 2007.
[46]	Chen, P.Y., Wu, C.Y.C., Clemons, G.A., Citadin, C.T., Silva, A.C., Possoit, H.E., Krzywanski, D.M. “Stearic Acid Methyl Ester Affords Neuroprotection and Improves Functional Outcomes after Cardiac Arrest”, Prostaglandins, Leukotrienes and Essential Fatty Acids, 159(2020). 1-7. August 2020.
[47]	García-Cerro, S., Rueda, N., Vidal, V., Puente, A., Campa, V., Lantigua, S., Narcís, O., Velasco, A., Bartesaghi, R., & Martínez-Cué, C. “Prenatal Administration of Oleic Acid or Linolenic Acid Reduces Neuromorphological and Cognitive Alterations in Ts65dn Down Syndrome Mice”, The Journal of Nutrition, 150(6). 1631-1643. June 2020.
[48]	Conrad, C.D., Ortiz, J.B., Judd, J.M. “Chronic stress and hippocampal dendritic complexity: Methodological and functional considerations”, Physiology & Behavior, 178. 66-81. September 2017.
[49]	McEwen, B.S., Sapolsky, R.M. “Stress and cognitive function”, Current Opinion in Neurobiology, 5(2). 205-216. April 1995.
[50]	Drenska, D., Varadinova, M., Boyadjieva, N., Bozhilova-Pastirova, A. “Effect of anthocyanins and mianserin on neuronal density in rat hippocampus in a model of oxidative stress”, Pharmacology online, 2. 133-138. 2008.
[51]	Galea, L.A. “Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents”, Brain Research Reviews, 57(2). 332-341. March 2008.
[52]	Arauchi, R., Hashioka, S., Tsuchie, K., Miyaoka, T., Tsumori, T., Limoa, E., Horiguchi, J. “Gunn rats with glial activation in the hippocampus show prolonged immobility time in the forced swimming test and tail suspension test”, Brain and Behavior, 8(8). 1-9. June 2018.
[53]	Hashioka, S., Klegeris, A., Mcgeer, P.L. “Proton pump inhibitors reduce interferon-γ-induced neurotoxicity and STAT3 phosphorylation of human astrocytes”, Glia, 59(5). 833-840. Febrary 2011.
[54]	Mosca, F., Hidalgo, G.I., Villasante, J., Almajano, M.P. “Continuous or batch solid-liquid extraction of antioxidant compounds from seeds of Sterculia apetala plant and kinetic release study”, Molecules, 23(7). 1-12. July 2018.
[55]	Mansouri, M.T., Soltani, M., Naghizadeh, B., Farbood, Y., Mashak, A., Sarkaki, A. “A possible mechanism for the anxiolytic-like effect of gallic acid in the rat elevated plus maze”, Pharmacology Biochemistry and Behavior, 117. 40-46. February 2014.