Una feromona de alarma produce reacción de congelamiento después de una sola exposición

Manuel Saldaña-Aguado, Ana G. Gutiérrez-García, Carlos M. Contreras

Resumen


Los sistemas sensoriales permiten integrar estímulos y evocar respuestas ante situaciones de amenaza o peligro para favorecer la supervivencia. La 2-heptanona es una feromona de alarma identificada en varias especies y su acción se establece de inmediato, provocando reacciones de evitación y de huida. Dado que se desconoce su acción en el largo plazo, el objetivo de este estudio fue evaluar las conductas desplegadas por ratas macho (n= 24) en el laberinto de brazos elevados (LBE), en la prueba de enterramiento defensivo (ED) y en la prueba de campo abierto (CA). Usamos 3 grupos de ratas, un grupo fue expuesto a estimulación olfativa mediante un flujo de 1.5 l/min de aire impregnado con 3 µl de 2-heptanona. Otro grupo fue sometido a estrés mediante estímulos auditivos impredecibles (4 kHz, 75 dB). Un tercer grupo se empleó como control (sin estimulación sensorial). Las pruebas conductuales se realizaron 24 horas después de la estimulación sensorial. La exposición a 2-heptanona incrementó el tiempo de permanencia en brazos cerrados en el LBE (p<0.05) una reacción considerada ansiosa y el congelamiento en el ED (p<0.05), una respuesta adaptativa. No se encontraron diferencias en CA. La estimulación auditiva no produjo efectos conductuales observables 24h después de la exposición. En conclusión, la 2-heptanona permite la expresión de un comportamiento adaptativo para afrontar situaciones de amenaza, mediante el congelamiento lo que permite ser menos detectable por posibles predadores. La aportación, es que tal conducta ocurre aún 24h después de la exposición.

 

Abstract: Sensory systems allow individuals to integrate stimuli and evoke responses in situations of threat or danger to favor survival. 2-heptanone is an alarm pheromone that has been identified in different species and its effect is immediately, producing avoidance and flight reactions. However, long term effects of this compound remain unknown. The aim of present study consists on determine and compare the long-term actions of this compound with auditory stimulation. We evaluated the behaviors displayed by male rats (n= 24) in the elevated plus maze, the defensive burying test and in the open field test, 24h after exposure. We used 3 groups of rats: one group was exposed to olfactory stimulation by a constant flow of 1.5 l/min of 3 µl 2-heptanone impregnated air. Another group was exposed to stress, using unpredictable auditory stimuli (4 kHz, 75 dB), a third group was used as control (without sensory stimulation). The behavioral tests were performed 24h after sensory stimulation. The 2-heptanone olfactory exposure increased the time spent in closed arms during the elevated plus maze (p<0.05), an anxiety like reaction, and freezing during the defensive burying test (p<0.05), an adaptative response. We did not observe differences in the open field test. No measurable behavioral effects were shown by the auditory stimulation group 24h after exposure. In conclusion, 2-heptanone allows the expression of an adaptative behavior to face a threatening situation by freezing, what makes subjects to be lees detectable to predators, this response lasts more than 24h after exposure.

Keywords: Fear; anxiety; freezing; 2-heptanone; olfactory system.


Palabras clave


Miedo; ansiedad; congelamiento; 2-heptanona; sistema olfativo.

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Referencias


Gutiérrez-García AG, Contreras CM. Algunos aspectos etológicos de la comunicación química en ratas y ratones de laboratorio. Rev Biomed 2002 13: 189-209.

Davis RL. Olfactory Learning. Neuron 2004 44(1): 31-48.

Takahashi L. Olfactory systems and neural circuits that modulate predator odor fear. Front Behav Neurosci. 2014 8: 72.

Mouly AM, Sullivan R. Memory and Plasticity in the Olfactory System: from infancy to adulthood. Front Neurosci, The Neurobiology of Olfaction. CRC Press/Taylor & Francis. 2009 pp367–39.

Perry RE, Al Aïn S, Raineki C, Sullivan RM, Wilson DA. Development of odor hedonics: Experience-dependent ontogeny of circuits supporting maternal and predator odor responses in rats. J Neurosci 2016 36(25) :6634-50.

Willander J, Larsson M. Olfaction and emotion: The case of autobiographical memory. Mem Cognit 2007 35(7): 1659-63.

Palmer A, Ress A, Malmierca MS, Hackett TA. Structural organization of the ascending auditory pathway. The Oxford Handbook of Auditory Science: The Auditory Brain. Oxford University Press, 2010.

Asaba A, Hattori T, Mogi K, Kikusui T. Sexual attractiveness of male chemicals and vocalizations in mice. Front Neurosci 2014 8: 231.

Bergman P, Västfjäll D, Tajadura-Jiménez A, Asutay E. Auditory-induced emotion mediates perceptual categorization of everyday sounds. Front Psychol 2016 7: 1565.

Wang JQ, Nicol T, Skoe E, Sams M, Kraus N. Emotion and the auditory brainstem response to speech. Neurosci lett 2010 469(3): 319-323.

Charitidi K., Canlon B. Estrogen receptors in the central auditory system of male and female mice. Neuroscience 2010 165(3): 923-33.

Oatley K, Jenkins,J. Understanding emotions. Blackwell Publ, USA. 1996 pp 23-26.

LeDoux J. Emotion circuits in the brain. Annu Rev Neurosci 2000 23: 155–184.

Contreras-García CM. Exposure to an alarm pheromone combined with footshock stress enhances responsivity of the medial amygdala-hippocampus circuit. Am J Psychiatry and Neurosci 2014 2(6): 83-88.

Herry C, Bach DR, Esposito F, Di Salle F, Perrig WJ, Scheffler K, Luthi A, Seifritz E. Processing of temporal unpredictability in human and animal amygdala. J Neurosci 2007 27(22): 5958–66.

Gutiérrez-García AG, Contreras CM. Algunos aspectos etológicos de la comunicación química en ratas y ratones de laboratorio. Rev Biomed 2002 13: 189-209.

Gutiérrez-García AG, Contreras CM, Mendoza M., Cruz S, García O, Rodríguez J, Bernal B. A single session of emotional stress produces anxiety in Wistar rats. Behav Brain Res 2006 167(1): 30-5.

Contreras CM, Gutiérrez-García AG, Molina T, Mendoza R. 2-Heptanone increases the firing rate of the basal amygdala: role of anterior olfactory epithelial organs. Neuropsychobiology 2012 66(3): 167-73.

Norma Oficial Mexicana NOM-062-ZOO-1999. Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. México, D.F.: Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación.

Handley SL, Mithani S. Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of fear-motivated behaviour. Naunyn Schmiedebergs Arch Pharmacol 1984 327(1): 1-5.

Pinel JP, Treit D. Burying as a defensive response in rats. J Comp Physiol Psychol 1978 92(4): 708-712.

Hall CS. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. Am Psychol Assoc 1934 18 (3): 385–403.

Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2007 2(2):322–328.

Martínez L, Estrada E, López C, Contreras CM., Fernández-Guasti A. Interaction of desipramine with steroid hormones on experimental anxiety. Psychoneuroendocrinology 2000 25(2): 109-20.

Hogg S. A Review of the Validity and Variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 1996 54(1): 21-30.

Pawlak CR, Karrenbauer BD, Schneider P, Ho YJ. The elevated plus-maze test: differential psychopharmacology of anxiety-related behavior. Emotion Review 2012 4(1): 98–115.

Sandbak T, Murison R. Behavioural responses to elevated plus-maze and defensive burying testing: effects on subsequent ethanol intake and effect of ethanol on retention of the burying response. Alcohol and Alcoholism 2001 36(1): 48-58.

Korte SM, De Boer SF, Bohus B. Fear-potentiation in the elevated plus-maze test depends on stressor controllability and fear conditioning. Stress 1999 3(1): 27–40.

Korte SM, De Boer SF. A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. Eur J Pharmacol 2003 463(1-3): 163-75.

De Boer SF, Koolhaas JM. Defensive burying in rodents: ethology, neurobiology and psychopharmacology. Eur J Pharmacol 2003 463(1-3): 145-61.

Hudson BB. One-trial learning in the domestic rat. Genet Psychol Monogr 1950 41: 99-145.

Fucich EA, Morilak DA. Shock-probe defensive burying test to measure active versus passive coping style in response to an aversive stimulus in rats. Bio Protoc 2018 8(17).

Roelofs K. Freeze for action: neurobiological mechanisms in animal and human freezing. Philos Trans R Soc Lond B Biol Sci 2017 372(1718).

Blanchard DC, Griebel G, Blanchard RJ. Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci Biobehav 2001 25(3): 205-18.

LeDoux JE, Iwata J, Cicchetti P, Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 1988 8(7): 2517-29.

Walker P, Carrive P. Role of ventrolateral periaqueductal gray neurons in the behavioral and cardiovascular responses to contextual conditioned fear and poststress recovery. Neuroscience 2003 116(3): 897–912. /span>

Blanchard DC, Griebel G, Pobbe, R, Blanchard RJ. Risk assessment as an evolved threat detection and analysis process. Neurosci Biobehav Rev 2011 35(4): 991-8.

Marx BP, Forsyth JP, Gallup GG, Fusé T, Lexington JM. Tonic immobility as an evolved predator defense: Implications for sexual assault survivors. Clinical Psychology Science and Practice 2008 15(1): 74–90.

Blanchard DC, Griebel G, Pobbe R, Blanchard RJ. Risk assessment as an evolved threat detection and analysis process. Neurosci Biobehav Rev 2011 35(4): 991-8.

Lapiz MD, Bondi CO, Doyen J, Rodriguez GA, Bédard T, Morilak DA. Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. J Neuroendocrinol 2008 20(10): 1115-37.

Seibenhener ML,Wooten MC. Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp 2015 (96):524-34.

Wang Y, Cao L, Lee CY, Matsuo T, Wu K, Asher G, Tang T, Russel J, Klewe-Nebenius D, Wang Li, Soya S, Hasegawa E, Chérasse Y, Yuwenbin T, Xiaowei W, Miyoshi C, Irukayama Y, Wang K, Sakurai T, Funato H, Yanagisawa M, Nagase H, Kobayakawa B, Qinghua L. Large-scale forward genetics screening identifies Trpa1 as a chemosensor for predator odor-evoked innate fear behaviors. Nat Commun 2018 9(1).

Fendt M, Endres T. 2,3,5-Trimethyl-3-thiazoline (TMT), a component of fox odor – Just repugnant or really fear-inducing? Neurosci Biobehav Rev 2008 32(7): 1259-66.

Brai E, Alberi L. Olfaction, among the first senses to develop and decline. En Sensory Nervous System. IntechOpen 2018: 65-99.

Stryjek R, Mioduszewska B, Spaltabaka-Gędek E, Juszczak GR. Wild Norway rats do not avoid predator scents when collecting food in a familiar habitat: a field study. Sci Rep 2018 8(1): 9475.




DOI: https://doi.org/10.25009/eb.v11i26.2551

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