Exposure to an Alarm Pheromone Combined with Footshock Stress Enhances Responsivity of the Medial Amygdala-Hippocampus Circuit
American Journal of Psychiatry and Neuroscience
Volume 2, Issue 6, November 2014, Pages: 83-89
Received: Nov. 11, 2014; Accepted: Nov. 19, 2014; Published: Nov. 23, 2014
Views 3002      Downloads 160
Carlos M. Contreras, Unidad Periférica del Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Xalapa, Veracruz, 91190, México; Laboratorio de Neurofarmacología, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, 91190, México
Tania Molina-Jiménez, Laboratorio de Neurofarmacología, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, 91190, México
Ana G. Gutiérrez-García, Laboratorio de Neurofarmacología, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, 91190, México; Facultad de Psicología, Universidad Veracruzana, Xalapa, Veracruz, 91097, México
Article Tools
Follow on us
Alarm substances are released under stressful situations and may constitute signals that prevent other members of the group from encountering dangerous situations by producing fear. 2-Heptanone is an alarm pheromone that increases the neuronal firing rate in temporal lobe structures that are related to fear in the rat, such as the basal amygdala. A single stress session of unavoidable electric footshock or 2-heptanone sniffing increases the responsivity of the medial amygdala-hippocampus circuit, but unknown is the timing of action of simultaneous exposure to both stressors on the firing rate and responsivity of CA1-CA3 neurons identified by their connections with the medial amygdala nucleus. Twenty-four or 48 h after a single stress session, we obtained single-unit extracellular recordings. The firing rate was higher in the 48 h group. The peristimulus histogram showed an increase in the responsivity of amygdala-hippocampus neurons, which was more pronounced 48 h after a single stress session. The present results suggest an increase in the sensitivity of this circuit after a single stress session, seemingly representing a first step in the formation of emotional memories related to a conditioned response to fear.
2-heptanone, Fear, Footshock, Amygdala, Hippocampus
To cite this article
Carlos M. Contreras, Tania Molina-Jiménez, Ana G. Gutiérrez-García, Exposure to an Alarm Pheromone Combined with Footshock Stress Enhances Responsivity of the Medial Amygdala-Hippocampus Circuit, American Journal of Psychiatry and Neuroscience. Vol. 2, No. 6, 2014, pp. 83-89. doi: 10.11648/j.ajpn.20140206.11
K. Ackerl, M. Atzmueller, K. Grammer. “The scent of fear”. Neuroendocrinol Lett, 23:79-84, 2002.
J. Albrecht, M. Demmel, V Schöpf, A.M. Kleemann, R. Kopietz, J. May, T. Schereder, R. Zernecke, H. Brückmann, M. Wiesmann. “Smelling chemosensory signals of males in anxious versus nonaxious condition increases state anxiety of female subjects”. Chem Senses, 36:19-27, 2010.
R.H. Pastel. “Collective behaviors: mass panic and outbreaks of multiple unexplained symptoms”. Mil Med, 166:44-46, 2001.
A.R. Mawson. “Understanding mass panic and other collective responses to threat and disaster”. Psychiatry, 68:95-113, 2005.
J.S. Morris, C.D. Frith, D.I. Perrett, D. Rowland, A.W. Young, A.J. Calder, R.J. Dolan. “A differential neural response in the human amygdala to fearful and happy facial expressions”. Nature, 383:812-815, 1996.
E.A. Krusemark, L.R. Novak, D.R. Gitelman, W. Li. “When the sense of smell meets emotion: anxiety-state-dependent olfactory processing and neural circuitry adaptation”. J Neurosci, 33:15324-15332, 2013.
E.A. Phelps. “Human emotional and memory: interaction of the amygdala and hippocampal complex”. Curr Opin Neurobiol, 14:198-202, 2002.
R. Paz, D. Pare. “Physiological basis for emotional modulation of memory circuits by the amygdala”. Curr Opin Neurobiol, 23:381-386, 2013.
N. Gutiérrez-Castellanos, A. Martínez-Marcos, F. Martínez-García, E. Lanuza. “Chemosensory function of the amygdala”. Vitam Horm, 83:165-196, 2010.
R. Hauser, M. Wiergowski, M. Kaliszan, T. Gos, G. Kernbach-Wighton, M. Studniarek, Z. Jankowski, J. Namieśnik. “Olfactory and tissue markers of fear in mammals including humans”. Med Hypotheses, 77:1062-1067, 2011.
B. de Lacy Costello, A. Amann, H. Al-Kateb, C. Flynn, W. Filipiak, T. Khalid, D. Osborne, N.M. Ratcliffe. “A review of the volatiles from the healthy human body”. J Breath Res, 8:014001, 2014.
AG. Gutiérrez-García, C.M Contreras, R. Mendoza-López, S. Cruz-Sánchez, O. García-Barradas, J.F. Rodríguez-Landa, B. Bernal-Morales. “A single session of emotional stress produces anxiety in Wistar rats”. Behav Brain Res, 167:30-35, 2006.
A.G. Gutiérrez-García, C.M. Contreras, R. Mendoza-López, O. García-Barradas, S. Cruz-Sánchez. “Urine from stressed rats increases immobility in receptor rats forced to swim: role of 2-heptanone”. Physiol Behav, 91:166-172, 2007.
C.M. Contreras, A.G. Gutiérrez-García, T. Molina-Jiménez, R. Mendoza-López. “2-Heptanone increases the firing rate of the basal amygdala: role of anterior olfactory epithelial organs”. Neuropsychobiology, 66:167-173, 2012.
C.M. Contreras, A.G. Gutiérrez-García, T. Molina-Jiménez. “Anterior olfactory organ removal produces anxiety-like behavior and increases spontaneous neuronal firing rate in basal amygdala”. Behav Brain Res, 252:101-119, 2013.
G. Richter-Levin, I. Akirav I. “Amygdala-hippocampus dynamic interaction in relation to memory”. Mol Neurobiol, 22:11-20, 2000.
K. Abe. “Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory”. Jpn J Pharmacol, 86:18-22, 2001.
G. Richter-Levin, I. Akirav I. “Emotional tagging of memory formation: in the search for neural mechanisms”. Brain Res Brain Res Rev, 43:247-256, 2003.
C.I. Li, T.L. Maglinao, L.K. Takahashi. “Medial amygdala modulation of predator odor-induced unconditioned fear in the rat”. Behav Neurosci, 118:324-332, 2004.
M. Müller, M. Fendt. “Temporary inactivation of the medial and basolateral amygdala differentially affects TMT-induced fear behavior in rats”. Behav Brain Res, 167:57-62, 2006.
S. Campeau, T.J. Nyhuis, S.K. Sasse, H.E. Day, C.V. Masini. “Acute and chronic effects of ferret odor exposure in Sprague-Dawley rats”. Neurosci Biobehav Rev, 32:1277-1286, 2008.
P. Blier, C. de Montigny C. “Serotoninergic but not noradrenergic neurons in rat central nervous system adapt to long-term treatment with monoamine oxidase inhibitors”. Neuroscience, 16:949-955, 1985.
T. Molina-Jiménez, A.G. Gutiérrez-García, C.M. Contreras. “An alarm pheromone increases the responsivity of amygdaline-hippocampal neurons”. Salud Mental, 36:279-284, 2013.
National Research Council. Guide for the Care and Use of Laboratory Animals (publication no. 80-23). Washington DC: National Academy Press; 1996.
T. Leinders-Zufall, A.P. Lane, A.C. Puce, W. Ma, M. Novotny, M.T. Shipley, F. Zufall. “Ultrasensitive pheromone detection by mammalian vomeronasal neurons”. Nature, 405:792-796, 2000.
R.G. Phillips, J.E. LeDoux. “Differential contributions of amygdala and hippocampus to cued and contextual fear conditioning”. Behav Neurosci, 106:274-285, 1992.
J.M. Santos, A.C. Gárgaro, A.R. Oliveira, S. Masson, M.L. Brandão. “Pharmacological dissociation of moderate and high contextual fear as assessed by freezing behavior and fear-potentiated startle”. Eur Neuropsychopharmacol, 15:239-246, 2005.
M. Sánchez-Alvarez, M. León-Olea, M. Condés-Lara, M. Briones, A. Fernández-Guardiola. “Localization of the microelectrode tip combining a rapid procedure method and marking with pontamine sky blue”. Bol Estud Med Biol, 36:55-59, 1988.
G. Paxinos, C. Watson. “The rat brain in stereotaxic coordinates”, 4th edition. San Diego: Academic Press; 1998.
E. Thomas, M. DeWolfe, F. Sancar, N. Todi, E. Yadin. “Electrophysiological analysis of the interaction between the lateral septum and the central nucleus of the amygdala”. Neurosci Lett, 524:79-83, 2012.
S. Frey, J. Bergado-Rosado, T. Seidenbecker, H.C. Pape, J.U. Frey. “Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP”. J Neurosci, 21:3697-3703, 2001.
F. Scalia, S.S. Winans. “The differential projections of the olfactory bulb and accessory olfactory bulb in mammals”. J Comp Neurol, 161:31-55, 1975.
N.S. Canteras, R.B. Simerly, L.W. Swanson. “Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat”. J Comp Neurol, 360:213-245, 1995.
V.R. Heale, C.H. Vanderwolf, M. Kavaliers. “Components of weasel and fox odors elicit fast wave bursts in the dentate gyrus of rats”. Behav Brain Res, 63:159-165, 1994.
H.C. Dringenberg, D. Oliveira, D. Habib. “Predator (cat hair)-induced enhancement of hippocampal long-term potentiation in rats: involvement of acetylcholine”. Learn Mem, 15:112-116, 2008.
J.E. LeDoux. “Evolution of human emotion: a view through fear”. Prog Brain Res, 195:431-442, 2012.
A.J. McDonald. “Cortical phatways to the mammalian amygdala”. Prog Neurobiol, 55:257-332, 1998.
D.C. Blanchard, G. Griebel, R.J. Blanchard. “Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion”. Prog Neuropsychopharmacol Biol Psychiatry, 27:1177-1185, 2003.
R. Hauser, M. Marczak, B. Karaszewski, M. Wiergowski, M. Kaliszan, M. Penkowski, G. Kernbach-Wighton, Z. Jankowski, J. Namieśnik. “A preliminary study for identifying olfactory markers of fear in the rat”. Lab Anim, 37:76-80, 2008.
Y. Kiyokawa, T. Kikusui, Y. Takeuchi, Y. Mori. “Mapping the neural circuit activated by alarm pheromone perception by c-Fos immunohistochemistry”. Brain Res, 1043:145-154, 2005.
N. Maggio, M. Segal. “Differential modulation of long-term depression by acute stress in the rat dorsal and ventral hippocampus”. J Neurosci, 29:8633-8638, 2009.
D. Caudal, B.P. Godsil, F. Mailliet, D. Bergerot, T.M. Jay. “Acute stress induces contrasting changes in AMPA receptor subunit phosphorylation within the prefrontal cortex, amygdala and hippocampus”. PLoS One, 5:e1528, 2010.
C. Weiss, E. Sametsky, A. Sasse, J. Spiess, J.F. Disterhoft. “Acute stress facilitates trace eyeblink conditioning in C57BL/6 male mice and increases the excitability of their CA1 pyramidal neurons”. Learn Mem, 12:138-143, 2005.
Z. Wang, RD. Pang, M. Hernandez, MA Ocampo, D.P. Holschneider. “Anxiolytic-like effect of pregabalin on unconditioned fear in the rat: an autoradiographic brain perfusion mapping and functional connectivity study”. Neuroimage, 59:4168-4188, 2012.
M.S. Fanselow, H.W. Dong. “Are the dorsal and ventral hippocampus functionally distinct structures” Neuron, 65:7-19, 2010.
D.M. Bannerman, J.N. Rawlins, S.B. McHugh, R.M. Deacon, B.K. Yee, T. Bast, W.N. Zhang, H.H. Pothuizen, J. Feldon. “Regional dissociations within the hippocampus: memory and anxiety”. Neurosci Biobehav Rev, 28:273-283, 2004.
F. Zufall, S.D. Munger. “From odor and pheromone transduction to the organization of the sense of smell”. Trends Neurosci, 24:191-193, 2001.
G.Y. Paschall, M. Davis. “Second-order olfactory-mediated fear-potentiated startle”. Learn Mem, 9:395-401, 2002.
N. Sakai, S. Imada. “Bilateral lesions of the insular cortex or of the prefrontal cortex block the association between taste and odor in the rat”. Neurobiol Learn Mem, 80:24-31, 2003.
J.A. Kroon, A.P. Carobrez. “Olfactory fear conditioning paradigm in rats: effects of midazolam, propranolol or scopolamine”. Neurobiol Learn Mem, 91:32-40, 2009.
L.K. Takahashi, D.T. Hubbard, I. Lee, Y. Dar, S.M. Sipes. “Predator odor-induced conditioned fear involves the basolateral and medial amygdala”. Behav Neurosci, 121:100-110, 2007.
L.K. Takahashi, M.M Chan, M.L. Pilar. “Predator odor fear conditioning: current perspectives and new directions”. Neurosci Biobehav, 32:1218-1227, 2008.
S.K. Baisley, C.L. Cloninger, V.P. Bakshi. “Fos expression following regimens of predator stress versus footshock that differentially affect prepulse inhibition in rats”. Physiol Behav, 104:796-803, 2011.
T.V. Bliss, G.L. Collingridge. “A synaptic model of memory: long-term potentiation in the hippocampus”. Nature, 361:31-39, 1993.
U. Frey, Y.Y. Huang, E.R. Kandel. “Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons”. Science, 260:1661-1664, 1993.
T.V. Bliss, T. Lomo. “Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path”. J Physiol , 232:331-356, 1973.
T.W Berger. “Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning”. Science, 224:627-630, 1984.
Science Publishing Group
1 Rockefeller Plaza,
10th and 11th Floors,
New York, NY 10020
Tel: (001)347-983-5186