Skip to main content
Top
Published in: NeuroMolecular Medicine 3/2015

01-09-2015 | Original Paper

Alpha-Linolenic Acid-Induced Increase in Neurogenesis is a Key Factor in the Improvement in the Passive Avoidance Task After Soman Exposure

Authors: Tetsade CB Piermartiri, Hongna Pan, Jun Chen, John McDonough, Neil Grunberg, James P. Apland, Ann M. Marini

Published in: NeuroMolecular Medicine | Issue 3/2015

Login to get access

Abstract

Exposure to organophosphorous (OP) nerve agents such as soman inhibits the critical enzyme acetylcholinesterase (AChE) leading to excessive acetylcholine accumulation in synapses, resulting in cholinergic crisis, status epilepticus and brain damage in survivors. The hippocampus is profoundly damaged after soman exposure leading to long-term memory deficits. We have previously shown that treatment with three sequential doses of alpha-linolenic acid, an essential omega-3 polyunsaturated fatty acid, increases brain plasticity in naïve animals. However, the effects of this dosing schedule administered after a brain insult and the underlying molecular mechanisms in the hippocampus are unknown. We now show that injection of three sequential doses of alpha-linolenic acid after soman exposure increases the endogenous expression of mature BDNF, activates Akt and the mammalian target of rapamycin complex 1 (mTORC1), increases neurogenesis in the subgranular zone of the dentate gyrus, increases retention latency in the passive avoidance task and increases animal survival. In sharp contrast, while soman exposure also increases mature BDNF, this increase did not activate downstream signaling pathways or neurogenesis. Administration of the inhibitor of mTORC1, rapamycin, blocked the alpha-linolenic acid-induced neurogenesis and the enhanced retention latency but did not affect animal survival. Our results suggest that alpha-linolenic acid induces a long-lasting neurorestorative effect that involves activation of mTORC1 possibly via a BDNF-TrkB-mediated mechanism.
Literature
go back to reference Abe, O., Yamasue, H., Kasai, K., Yamada, H., Aoki, S., et al. (2006). Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism. Psychiatry Research, 146, 231–242.PubMed Abe, O., Yamasue, H., Kasai, K., Yamada, H., Aoki, S., et al. (2006). Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism. Psychiatry Research, 146, 231–242.PubMed
go back to reference Adachi, M., Barrot, M., Autry, A. E., Theobald, D., & Monteggia, L. M. (2008). Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biological Psychiatry, 63, 642–649.PubMedCentralPubMed Adachi, M., Barrot, M., Autry, A. E., Theobald, D., & Monteggia, L. M. (2008). Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biological Psychiatry, 63, 642–649.PubMedCentralPubMed
go back to reference Ahn, Y. J., Park, S. J., Woo, H., Lee, H. E., Kim, H. J., et al. (2014). Effects of allantoin on cognitive function and hippocampal neurogenesis. Food and Chemical Toxicology, 64, 210–216.PubMed Ahn, Y. J., Park, S. J., Woo, H., Lee, H. E., Kim, H. J., et al. (2014). Effects of allantoin on cognitive function and hippocampal neurogenesis. Food and Chemical Toxicology, 64, 210–216.PubMed
go back to reference Aimone, J. B., Wiles, J., & Gage, F. H. (2006). Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neuroscience, 9, 723–727.PubMed Aimone, J. B., Wiles, J., & Gage, F. H. (2006). Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neuroscience, 9, 723–727.PubMed
go back to reference Alderson, R. F., Alterman, A. L., Barde, Y. A., & Lindsay, R. M. (1990). Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron, 5, 297–306.PubMed Alderson, R. F., Alterman, A. L., Barde, Y. A., & Lindsay, R. M. (1990). Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron, 5, 297–306.PubMed
go back to reference Aroniadou-Anderjaska, V., Figueiredo, T. H., Apland, J. P., Qashu, F., & Braga, M. F. (2009). Primary brain targets of nerve agents: The role of the amygdala in comparison to the hippocampus. Neurotoxicology, 30, 772–776.PubMedCentralPubMed Aroniadou-Anderjaska, V., Figueiredo, T. H., Apland, J. P., Qashu, F., & Braga, M. F. (2009). Primary brain targets of nerve agents: The role of the amygdala in comparison to the hippocampus. Neurotoxicology, 30, 772–776.PubMedCentralPubMed
go back to reference Bajgar, J. (2005). Complex view on poisoning with nerve agents and organophosphates. Acta Medica (Hradec Kralove), 48, 3–21. Bajgar, J. (2005). Complex view on poisoning with nerve agents and organophosphates. Acta Medica (Hradec Kralove), 48, 3–21.
go back to reference Ballarin, M., Ernfors, P., Lindefors, N., & Persson, H. (1991). Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Experimental Neurology, 114, 35–43.PubMed Ballarin, M., Ernfors, P., Lindefors, N., & Persson, H. (1991). Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Experimental Neurology, 114, 35–43.PubMed
go back to reference Bateman, J. M., & McNeill, H. (2004). Temporal control of differentiation by the insulin receptor/tor pathway in Drosophila. Cell, 119, 87–96.PubMed Bateman, J. M., & McNeill, H. (2004). Temporal control of differentiation by the insulin receptor/tor pathway in Drosophila. Cell, 119, 87–96.PubMed
go back to reference Bergami, M., Berninger, B., & Canossa, M. (2009). Conditional deletion of TrkB alters adult hippocampal neurogenesis and anxiety-related behavior. Communicative and Integrative Biology, 2, 14–16.PubMedCentralPubMed Bergami, M., Berninger, B., & Canossa, M. (2009). Conditional deletion of TrkB alters adult hippocampal neurogenesis and anxiety-related behavior. Communicative and Integrative Biology, 2, 14–16.PubMedCentralPubMed
go back to reference Binder, D. K., Croll, S. D., Gall, C. M., & Scharfman, H. E. (2001). BDNF and epilepsy: Too much of a good thing? Trends in Neurosciences, 24, 47–53.PubMed Binder, D. K., Croll, S. D., Gall, C. M., & Scharfman, H. E. (2001). BDNF and epilepsy: Too much of a good thing? Trends in Neurosciences, 24, 47–53.PubMed
go back to reference Blondeau, N., Nguemeni, C., Debruyne, D. N., Piens, M., Wu, X., et al. (2009). Subchronic alpha-linolenic acid treatment enhances brain plasticity and exerts an anti-depressant effect: A versatile potential therapy for stroke. Neuropsychopharmacology, 34, 2548–2559.PubMed Blondeau, N., Nguemeni, C., Debruyne, D. N., Piens, M., Wu, X., et al. (2009). Subchronic alpha-linolenic acid treatment enhances brain plasticity and exerts an anti-depressant effect: A versatile potential therapy for stroke. Neuropsychopharmacology, 34, 2548–2559.PubMed
go back to reference Blondeau, N., Widmann, C., Lazdunski, M., & Heurteaux, C. (2002). Polyunsaturated fatty acids induce ischemic and epileptic tolerance. Neuroscience, 109, 231–241.PubMed Blondeau, N., Widmann, C., Lazdunski, M., & Heurteaux, C. (2002). Polyunsaturated fatty acids induce ischemic and epileptic tolerance. Neuroscience, 109, 231–241.PubMed
go back to reference Bovolenta, R., Zucchini, S., Paradiso, B., Rodi, D., Merigo, F., et al. (2010). Hippocampal FGF-2 and BDNF overexpression attenuates epileptogenesis-associated neuroinflammation and reduces spontaneous recurrent seizures. Journal of Neuroinflammation, 7, 81.PubMedCentralPubMed Bovolenta, R., Zucchini, S., Paradiso, B., Rodi, D., Merigo, F., et al. (2010). Hippocampal FGF-2 and BDNF overexpression attenuates epileptogenesis-associated neuroinflammation and reduces spontaneous recurrent seizures. Journal of Neuroinflammation, 7, 81.PubMedCentralPubMed
go back to reference Buccafusco, J. J., Heithold, D. L., & Chon, S. H. (1990). Long-term behavioral and learning abnormalities produced by the irreversible cholinesterase inhibitor soman: Effect of a standard pretreatment regimen and clonidine. Toxicology Letters, 52, 319–329.PubMed Buccafusco, J. J., Heithold, D. L., & Chon, S. H. (1990). Long-term behavioral and learning abnormalities produced by the irreversible cholinesterase inhibitor soman: Effect of a standard pretreatment regimen and clonidine. Toxicology Letters, 52, 319–329.PubMed
go back to reference Buckmaster, P. S., & Lew, F. H. (2011). Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. Journal of Neuroscience, 31, 2337–2347.PubMedCentralPubMed Buckmaster, P. S., & Lew, F. H. (2011). Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. Journal of Neuroscience, 31, 2337–2347.PubMedCentralPubMed
go back to reference Cameron, H. A., & McKay, R. D. (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. The Journal of Comparative Neurology, 435, 406–417.PubMed Cameron, H. A., & McKay, R. D. (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. The Journal of Comparative Neurology, 435, 406–417.PubMed
go back to reference Carpentier, P., Lambrinidis, M., & Blanchet, G. (1991). Early dendritic changes in hippocampal pyramidal neurones (field CA1) of rats subjected to acute soman intoxication: A light microscopic study. Brain Research, 541, 293–299.PubMed Carpentier, P., Lambrinidis, M., & Blanchet, G. (1991). Early dendritic changes in hippocampal pyramidal neurones (field CA1) of rats subjected to acute soman intoxication: A light microscopic study. Brain Research, 541, 293–299.PubMed
go back to reference Cheng, A., Wang, S., Cai, J., Rao, M. S., & Mattson, M. P. (2003). Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Developmental Biology, 258, 319–333.PubMed Cheng, A., Wang, S., Cai, J., Rao, M. S., & Mattson, M. P. (2003). Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Developmental Biology, 258, 319–333.PubMed
go back to reference Choi, E. K., Park, D., Yon, J. M., Hur, G. H., Ha, Y. C., et al. (2004). Protection by sustained release of physostigmine and procyclidine of soman poisoning in rats. European Journal of Pharmacology, 505, 83–91.PubMed Choi, E. K., Park, D., Yon, J. M., Hur, G. H., Ha, Y. C., et al. (2004). Protection by sustained release of physostigmine and procyclidine of soman poisoning in rats. European Journal of Pharmacology, 505, 83–91.PubMed
go back to reference Clement, J. G., & Broxup, B. (1993). Efficacy of diazepam and avizafone against soman-induced neuropathology in brain of rats. Neurotoxicology, 14, 485–504.PubMed Clement, J. G., & Broxup, B. (1993). Efficacy of diazepam and avizafone against soman-induced neuropathology in brain of rats. Neurotoxicology, 14, 485–504.PubMed
go back to reference Collombet, J. M., Four, E., Bernabe, D., Masqueliez, C., Burckhart, M. F., et al. (2005). Soman poisoning increases neural progenitor proliferation and induces long-term glial activation in mouse brain. Toxicology, 208, 319–334.PubMed Collombet, J. M., Four, E., Bernabe, D., Masqueliez, C., Burckhart, M. F., et al. (2005). Soman poisoning increases neural progenitor proliferation and induces long-term glial activation in mouse brain. Toxicology, 208, 319–334.PubMed
go back to reference Cornu, M., Oppliger, W., Albert, V., Robitaille, A. M., Trapani, F., et al. (2014). Hepatic mTORC1 controls locomotor activity, body temperature, and lipid metabolism through FGF21. Proceedings of the National Academy of Sciences of the United States of America, 111, 11592–11599.PubMedCentralPubMed Cornu, M., Oppliger, W., Albert, V., Robitaille, A. M., Trapani, F., et al. (2014). Hepatic mTORC1 controls locomotor activity, body temperature, and lipid metabolism through FGF21. Proceedings of the National Academy of Sciences of the United States of America, 111, 11592–11599.PubMedCentralPubMed
go back to reference Costa-Mattioli, M., & Monteggia, L. M. (2013). mTOR complexes in neurodevelopmental and neuropsychiatric disorders. Nature Neuroscience, 16, 1537–1543.PubMed Costa-Mattioli, M., & Monteggia, L. M. (2013). mTOR complexes in neurodevelopmental and neuropsychiatric disorders. Nature Neuroscience, 16, 1537–1543.PubMed
go back to reference Dash, P. K., Orsi, S. A., & Moore, A. N. (2006). Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. The Journal of Neuroscience, 26, 8048–8056.PubMed Dash, P. K., Orsi, S. A., & Moore, A. N. (2006). Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. The Journal of Neuroscience, 26, 8048–8056.PubMed
go back to reference Deblon, N., Bourgoin, L., Veyrat-Durebex, C., Peyrou, M., Vinciguerra, M., et al. (2012). Chronic mTOR inhibition by rapamycin induces muscle insulin resistance despite weight loss in rats. British Journal of Pharmacology, 165, 2325–2340.PubMedCentralPubMed Deblon, N., Bourgoin, L., Veyrat-Durebex, C., Peyrou, M., Vinciguerra, M., et al. (2012). Chronic mTOR inhibition by rapamycin induces muscle insulin resistance despite weight loss in rats. British Journal of Pharmacology, 165, 2325–2340.PubMedCentralPubMed
go back to reference Deng, W., Saxe, M. D., Gallina, I. S., & Gage, F. H. (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. The Journal of Neuroscience, 29, 13532–13542.PubMedCentralPubMed Deng, W., Saxe, M. D., Gallina, I. S., & Gage, F. H. (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. The Journal of Neuroscience, 29, 13532–13542.PubMedCentralPubMed
go back to reference Deng, W., Aimone, J. B., & Gage, F. H. (2010). New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nature Reviews Neuroscience, 11, 339–350.PubMedCentralPubMed Deng, W., Aimone, J. B., & Gage, F. H. (2010). New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nature Reviews Neuroscience, 11, 339–350.PubMedCentralPubMed
go back to reference Dupret, D., Revest, J. M., Koehl, M., Ichas, F., De Giorgi, F., et al. (2008). Spatial relational memory requires hippocampal adult neurogenesis. PLoS One, 3, e1959.PubMedCentralPubMed Dupret, D., Revest, J. M., Koehl, M., Ichas, F., De Giorgi, F., et al. (2008). Spatial relational memory requires hippocampal adult neurogenesis. PLoS One, 3, e1959.PubMedCentralPubMed
go back to reference Duvel, K., Yecies, J. L., Menon, S., Raman, P., Lipovsky, A. I., et al. (2010). Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Molecular Cell, 39, 171–183.PubMedCentralPubMed Duvel, K., Yecies, J. L., Menon, S., Raman, P., Lipovsky, A. I., et al. (2010). Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Molecular Cell, 39, 171–183.PubMedCentralPubMed
go back to reference Elmer, E., Kokaia, Z., Kokaia, M., Carnahan, J., Nawa, H., & Lindvall, O. (1998). Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience, 83, 351–362.PubMed Elmer, E., Kokaia, Z., Kokaia, M., Carnahan, J., Nawa, H., & Lindvall, O. (1998). Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience, 83, 351–362.PubMed
go back to reference Faivre, E., Gault, V. A., Thorens, B., & Holscher, C. (2011). Glucose-dependent insulinotropic polypeptide receptor knockout mice are impaired in learning, synaptic plasticity, and neurogenesis. Journal of Neurophysiology, 105, 1574–1580.PubMed Faivre, E., Gault, V. A., Thorens, B., & Holscher, C. (2011). Glucose-dependent insulinotropic polypeptide receptor knockout mice are impaired in learning, synaptic plasticity, and neurogenesis. Journal of Neurophysiology, 105, 1574–1580.PubMed
go back to reference Felix, M. S., Popa, N., Djelloul, M., Boucraut, J., Gauthier, P., et al. (2012). Alteration of forebrain neurogenesis after cervical spinal cord injury in the adult rat. Frontiers in Neuroscience, 6, 45.PubMedCentralPubMed Felix, M. S., Popa, N., Djelloul, M., Boucraut, J., Gauthier, P., et al. (2012). Alteration of forebrain neurogenesis after cervical spinal cord injury in the adult rat. Frontiers in Neuroscience, 6, 45.PubMedCentralPubMed
go back to reference Filliat, P., Baubichon, D., Burckhart, M. F., Pernot-Marino, I., Foquin, A., et al. (1999). Memory impairment after soman intoxication in rat: Correlation with central neuropathology. Improvement with anticholinergic and antiglutamatergic therapeutics. Neurotoxicology, 20, 535–549.PubMed Filliat, P., Baubichon, D., Burckhart, M. F., Pernot-Marino, I., Foquin, A., et al. (1999). Memory impairment after soman intoxication in rat: Correlation with central neuropathology. Improvement with anticholinergic and antiglutamatergic therapeutics. Neurotoxicology, 20, 535–549.PubMed
go back to reference Filliat, P., Coubard, S., Pierard, C., Liscia, P., Beracochea, D., et al. (2007). Long-term behavioral consequences of soman poisoning in mice. Neurotoxicology, 28, 508–519.PubMed Filliat, P., Coubard, S., Pierard, C., Liscia, P., Beracochea, D., et al. (2007). Long-term behavioral consequences of soman poisoning in mice. Neurotoxicology, 28, 508–519.PubMed
go back to reference Garcia-Calatayud, S., Redondo, C., Martin, E., Ruiz, J. I., Garcia-Fuentes, M., & Sanjurjo, P. (2005). Brain docosahexaenoic acid status and learning in young rats submitted to dietary long-chain polyunsaturated fatty acid deficiency and supplementation limited to lactation. Pediatric Research, 57, 719–723.PubMed Garcia-Calatayud, S., Redondo, C., Martin, E., Ruiz, J. I., Garcia-Fuentes, M., & Sanjurjo, P. (2005). Brain docosahexaenoic acid status and learning in young rats submitted to dietary long-chain polyunsaturated fatty acid deficiency and supplementation limited to lactation. Pediatric Research, 57, 719–723.PubMed
go back to reference Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., & Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron, 54, 559–566.PubMedCentralPubMed Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., & Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron, 54, 559–566.PubMedCentralPubMed
go back to reference Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J. D., & Lledo, P. M. (2000). Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proceedings of the National Academy of Sciences of the United States of America, 97, 1823–1828.PubMedCentralPubMed Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J. D., & Lledo, P. M. (2000). Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proceedings of the National Academy of Sciences of the United States of America, 97, 1823–1828.PubMedCentralPubMed
go back to reference Hagg, T. (2005). Molecular regulation of adult CNS neurogenesis: An integrated view. Trends in Neurosciences, 28, 589–595.PubMed Hagg, T. (2005). Molecular regulation of adult CNS neurogenesis: An integrated view. Trends in Neurosciences, 28, 589–595.PubMed
go back to reference Han, J., Wang, B., Xiao, Z., Gao, Y., Zhao, Y., et al. (2008). Mammalian target of rapamycin (mTOR) is involved in the neuronal differentiation of neural progenitors induced by insulin. Molecular and Cellular Neurosciences, 39, 118–124.PubMed Han, J., Wang, B., Xiao, Z., Gao, Y., Zhao, Y., et al. (2008). Mammalian target of rapamycin (mTOR) is involved in the neuronal differentiation of neural progenitors induced by insulin. Molecular and Cellular Neurosciences, 39, 118–124.PubMed
go back to reference Hartman, A. L., Santos, P., Dolce, A., & Hardwick, J. M. (2012). The mTOR inhibitor rapamycin has limited acute anticonvulsant effects in mice. PLoS One, 7, e45156.PubMedCentralPubMed Hartman, A. L., Santos, P., Dolce, A., & Hardwick, J. M. (2012). The mTOR inhibitor rapamycin has limited acute anticonvulsant effects in mice. PLoS One, 7, e45156.PubMedCentralPubMed
go back to reference Heinrich, C., Lahteinen, S., Suzuki, F., Anne-Marie, L., Huber, S., et al. (2011). Increase in BDNF-mediated TrkB signaling promotes epileptogenesis in a mouse model of mesial temporal lobe epilepsy. Neurobiology of Disease, 42, 35–47.PubMed Heinrich, C., Lahteinen, S., Suzuki, F., Anne-Marie, L., Huber, S., et al. (2011). Increase in BDNF-mediated TrkB signaling promotes epileptogenesis in a mouse model of mesial temporal lobe epilepsy. Neurobiology of Disease, 42, 35–47.PubMed
go back to reference Hentges, K. E., Sirry, B., Gingeras, A. C., Sarbassov, D., Sonenberg, N., et al. (2001). FRAP/mTOR is required for proliferation and patterning during embryonic development in the mouse. Proceedings of the National Academy of Sciences of the United States of America, 98, 13796–13801.PubMedCentralPubMed Hentges, K. E., Sirry, B., Gingeras, A. C., Sarbassov, D., Sonenberg, N., et al. (2001). FRAP/mTOR is required for proliferation and patterning during embryonic development in the mouse. Proceedings of the National Academy of Sciences of the United States of America, 98, 13796–13801.PubMedCentralPubMed
go back to reference Heurteaux, C., Laigle, C., Blondeau, N., Jarretou, G., & Lazdunski, M. (2006). Alpha-linolenic acid and riluzole treatment confer cerebral protection and improve survival after focal brain ischemia. Neuroscience, 137, 241–251.PubMed Heurteaux, C., Laigle, C., Blondeau, N., Jarretou, G., & Lazdunski, M. (2006). Alpha-linolenic acid and riluzole treatment confer cerebral protection and improve survival after focal brain ischemia. Neuroscience, 137, 241–251.PubMed
go back to reference Hoeffer, C. A., & Klann, E. (2010). mTOR signaling: At the crossroads of plasticity, memory and disease. Trends in Neurosciences, 33, 67–75.PubMedCentralPubMed Hoeffer, C. A., & Klann, E. (2010). mTOR signaling: At the crossroads of plasticity, memory and disease. Trends in Neurosciences, 33, 67–75.PubMedCentralPubMed
go back to reference Hofer, M. M., & Barde, Y. A. (1988). Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature, 331, 261–262.PubMed Hofer, M. M., & Barde, Y. A. (1988). Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature, 331, 261–262.PubMed
go back to reference Hohn, A., Leibrock, J., Bailey, K., & Barde, Y. A. (1990). Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature, 344, 339–341.PubMed Hohn, A., Leibrock, J., Bailey, K., & Barde, Y. A. (1990). Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature, 344, 339–341.PubMed
go back to reference Hom, J., Haley, R. W., & Kurt, T. L. (1997). Neuropsychological correlates of Gulf War syndrome. Archives of Clinical Neuropsychology, 12, 531–544.PubMed Hom, J., Haley, R. W., & Kurt, T. L. (1997). Neuropsychological correlates of Gulf War syndrome. Archives of Clinical Neuropsychology, 12, 531–544.PubMed
go back to reference Hong, J. G., Kim, D. H., Park, S. J., Kim, J. M., Cai, M., et al. (2011). The memory-enhancing effects of Kami-ondam-tang in mice. Journal of Ethnopharmacology, 137, 251–256.PubMed Hong, J. G., Kim, D. H., Park, S. J., Kim, J. M., Cai, M., et al. (2011). The memory-enhancing effects of Kami-ondam-tang in mice. Journal of Ethnopharmacology, 137, 251–256.PubMed
go back to reference Hou, J. G., Xue, J. J., Lee, M. R., Sun, M. Q., Zhao, X. H., et al. (2013). Compound K is able to ameliorate the impaired cognitive function and hippocampal neurogenesis following chemotherapy treatment. Biochemical and Biophysical Research Communications, 436, 104–109.PubMed Hou, J. G., Xue, J. J., Lee, M. R., Sun, M. Q., Zhao, X. H., et al. (2013). Compound K is able to ameliorate the impaired cognitive function and hippocampal neurogenesis following chemotherapy treatment. Biochemical and Biophysical Research Communications, 436, 104–109.PubMed
go back to reference Howell, J. J., Ricoult, S. J., Ben-Sahra, I., & Manning, B. D. (2013). A growing role for mTOR in promoting anabolic metabolism. Biochemical Society Transactions, 41, 906–912.PubMed Howell, J. J., Ricoult, S. J., Ben-Sahra, I., & Manning, B. D. (2013). A growing role for mTOR in promoting anabolic metabolism. Biochemical Society Transactions, 41, 906–912.PubMed
go back to reference Humpel, C., Wetmore, C., & Olson, L. (1993). Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience, 53, 909–918.PubMed Humpel, C., Wetmore, C., & Olson, L. (1993). Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience, 53, 909–918.PubMed
go back to reference Jaholkowski, P., Kiryk, A., Jedynak, P., Ben Abdallah, N. M., Knapska, E., et al. (2009). New hippocampal neurons are not obligatory for memory formation; cyclin D2 knockout mice with no adult brain neurogenesis show learning. Learning Memory, 16, 439–451.PubMed Jaholkowski, P., Kiryk, A., Jedynak, P., Ben Abdallah, N. M., Knapska, E., et al. (2009). New hippocampal neurons are not obligatory for memory formation; cyclin D2 knockout mice with no adult brain neurogenesis show learning. Learning Memory, 16, 439–451.PubMed
go back to reference Jessberger, S., Zhao, C., Toni, N., Clemenson, G. D, Jr, Li, Y., & Gage, F. H. (2007). Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. The Journal of Neuroscience, 27, 9400–9407.PubMed Jessberger, S., Zhao, C., Toni, N., Clemenson, G. D, Jr, Li, Y., & Gage, F. H. (2007). Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. The Journal of Neuroscience, 27, 9400–9407.PubMed
go back to reference Jobim, P. F., Pedroso, T. R., Werenicz, A., Christoff, R. R., Maurmann, N., et al. (2012). Impairment of object recognition memory by rapamycin inhibition of mTOR in the amygdala or hippocampus around the time of learning or reactivation. Behavioural Brain Research, 228, 151–158.PubMed Jobim, P. F., Pedroso, T. R., Werenicz, A., Christoff, R. R., Maurmann, N., et al. (2012). Impairment of object recognition memory by rapamycin inhibition of mTOR in the amygdala or hippocampus around the time of learning or reactivation. Behavioural Brain Research, 228, 151–158.PubMed
go back to reference Joosen, M. J., Jousma, E., van den Boom, T. M., Kuijpers, W. C., Smit, A. B., et al. (2009). Long-term cognitive deficits accompanied by reduced neurogenesis after soman poisoning. Neurotoxicology, 30, 72–80.PubMed Joosen, M. J., Jousma, E., van den Boom, T. M., Kuijpers, W. C., Smit, A. B., et al. (2009). Long-term cognitive deficits accompanied by reduced neurogenesis after soman poisoning. Neurotoxicology, 30, 72–80.PubMed
go back to reference Katoh-Semba, R., Asano, T., Ueda, H., Morishita, R., Takeuchi, I. K., et al. (2002). Riluzole enhances expression of brain-derived neurotrophic factor with consequent proliferation of granule precursor cells in the rat hippocampus. FASEB Journal, 16, 1328–1330.PubMed Katoh-Semba, R., Asano, T., Ueda, H., Morishita, R., Takeuchi, I. K., et al. (2002). Riluzole enhances expression of brain-derived neurotrophic factor with consequent proliferation of granule precursor cells in the rat hippocampus. FASEB Journal, 16, 1328–1330.PubMed
go back to reference Kelleher, R. J, 3rd, Govindarajan, A., Jung, H. Y., Kang, H., & Tonegawa, S. (2004). Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell, 116, 467–479.PubMed Kelleher, R. J, 3rd, Govindarajan, A., Jung, H. Y., Kang, H., & Tonegawa, S. (2004). Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell, 116, 467–479.PubMed
go back to reference Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493–495.PubMed Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493–495.PubMed
go back to reference Kim, K. B., Nam, Y. A., Kim, H. S., Hayes, A. W., & Lee, B. M. (2014). Alpha-Linolenic acid: Nutraceutical, pharmacological and toxicological evaluation. Food and Chemical Toxicology, 70, 163–178.PubMed Kim, K. B., Nam, Y. A., Kim, H. S., Hayes, A. W., & Lee, B. M. (2014). Alpha-Linolenic acid: Nutraceutical, pharmacological and toxicological evaluation. Food and Chemical Toxicology, 70, 163–178.PubMed
go back to reference Kron, M. M., Zhang, H., & Parent, J. M. (2010). The developmental stage of dentate granule cells dictates their contribution to seizure-induced plasticity. The Journal of Neuroscience, 30, 2051–2059.PubMed Kron, M. M., Zhang, H., & Parent, J. M. (2010). The developmental stage of dentate granule cells dictates their contribution to seizure-induced plasticity. The Journal of Neuroscience, 30, 2051–2059.PubMed
go back to reference Kuhn, H. G., Dickinson-Anson, H., & Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. The Journal of Neuroscience, 16, 2027–2033.PubMed Kuhn, H. G., Dickinson-Anson, H., & Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. The Journal of Neuroscience, 16, 2027–2033.PubMed
go back to reference Lallement, G., Carpentier, P., Pernot-Marino, I., Baubichon, D., Collet, A., & Blanchet, G. (1991). Involvement of the different rat hippocampal glutamatergic receptors in development of seizures induced by soman: An autoradiographic study. Neurotoxicology, 12, 655–664.PubMed Lallement, G., Carpentier, P., Pernot-Marino, I., Baubichon, D., Collet, A., & Blanchet, G. (1991). Involvement of the different rat hippocampal glutamatergic receptors in development of seizures induced by soman: An autoradiographic study. Neurotoxicology, 12, 655–664.PubMed
go back to reference Lallement, G., Dorandeu, F., Filliat, P., Carpentier, P., Baille, V., & Blanchet, G. (1998). Medical management of organophosphate-induced seizures. Journal of physiology, 92, 369–373.PubMed Lallement, G., Dorandeu, F., Filliat, P., Carpentier, P., Baille, V., & Blanchet, G. (1998). Medical management of organophosphate-induced seizures. Journal of physiology, 92, 369–373.PubMed
go back to reference Lauritzen, I., Blondeau, N., Heurteaux, C., Widmann, C., Romey, G., & Lazdunski, M. (2000). Polyunsaturated fatty acids are potent neuroprotectors. The EMBO Journal, 19, 1784–1793.PubMedCentralPubMed Lauritzen, I., Blondeau, N., Heurteaux, C., Widmann, C., Romey, G., & Lazdunski, M. (2000). Polyunsaturated fatty acids are potent neuroprotectors. The EMBO Journal, 19, 1784–1793.PubMedCentralPubMed
go back to reference Lazarov, O., Mattson, M. P., Peterson, D. A., Pimplikar, S. W., & van Praag, H. (2010). When neurogenesis encounters aging and disease. Trends in Neurosciences, 33, 569–579.PubMedCentralPubMed Lazarov, O., Mattson, M. P., Peterson, D. A., Pimplikar, S. W., & van Praag, H. (2010). When neurogenesis encounters aging and disease. Trends in Neurosciences, 33, 569–579.PubMedCentralPubMed
go back to reference Lee, J., Duan, W., & Mattson, M. P. (2002). Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. Journal of Neurochemistry, 82, 1367–1375.PubMed Lee, J., Duan, W., & Mattson, M. P. (2002). Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. Journal of Neurochemistry, 82, 1367–1375.PubMed
go back to reference Lee, C. H., Kim, J. M., Kim, D. H., Park, S. J., Liu, X., et al. (2013a). Effects of Sun ginseng on memory enhancement and hippocampal neurogenesis. Phytotherapy Research, 27, 1293–1299.PubMed Lee, C. H., Kim, J. M., Kim, D. H., Park, S. J., Liu, X., et al. (2013a). Effects of Sun ginseng on memory enhancement and hippocampal neurogenesis. Phytotherapy Research, 27, 1293–1299.PubMed
go back to reference Lee, Y., Kim, J., Jang, S., & Oh, S. (2013b). Administration of phytoceramide enhances memory and upregulates the expression of pCREB and BDNF in hippocampus of Mice. Biomolecules and Therapeutics, 21, 229–233.PubMedCentralPubMed Lee, Y., Kim, J., Jang, S., & Oh, S. (2013b). Administration of phytoceramide enhances memory and upregulates the expression of pCREB and BDNF in hippocampus of Mice. Biomolecules and Therapeutics, 21, 229–233.PubMedCentralPubMed
go back to reference Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C. H., et al. (2008). TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron, 59, 399–412.PubMedCentralPubMed Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C. H., et al. (2008). TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron, 59, 399–412.PubMedCentralPubMed
go back to reference Li, N., Lee, B., Liu, R. J., Banasr, M., Dwyer, J. M., et al. (2010). mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science, 329, 959–964.PubMedCentralPubMed Li, N., Lee, B., Liu, R. J., Banasr, M., Dwyer, J. M., et al. (2010). mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science, 329, 959–964.PubMedCentralPubMed
go back to reference Lindholm, D., Dechant, G., Heisenberg, C. P., & Thoenen, H. (1993). Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. The European Journal of Neuroscience, 5, 1455–1464.PubMed Lindholm, D., Dechant, G., Heisenberg, C. P., & Thoenen, H. (1993). Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. The European Journal of Neuroscience, 5, 1455–1464.PubMed
go back to reference Lipsky, R. H., & Marini, A. M. (2007). Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Annals of the New York Academy of Sciences, 1122, 130–143.PubMed Lipsky, R. H., & Marini, A. M. (2007). Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Annals of the New York Academy of Sciences, 1122, 130–143.PubMed
go back to reference Lledo, P. M., Alonso, M., & Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nature Reviews Neuroscience, 7, 179–193.PubMed Lledo, P. M., Alonso, M., & Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nature Reviews Neuroscience, 7, 179–193.PubMed
go back to reference Magri, L., Cambiaghi, M., Cominelli, M., Alfaro-Cervello, C., Cursi, M., et al. (2011). Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions. Cell Stem Cell, 9, 447–462.PubMed Magri, L., Cambiaghi, M., Cominelli, M., Alfaro-Cervello, C., Cursi, M., et al. (2011). Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions. Cell Stem Cell, 9, 447–462.PubMed
go back to reference Marini, A. M., Rabin, S. J., Lipsky, R. H., & Mocchetti, I. (1998). Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-D-aspartate. The Journal of Biological Chemistry, 273, 29394–29399.PubMed Marini, A. M., Rabin, S. J., Lipsky, R. H., & Mocchetti, I. (1998). Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-D-aspartate. The Journal of Biological Chemistry, 273, 29394–29399.PubMed
go back to reference Marsden, W. N. (2012). Synaptic plasticity in depression: Molecular, cellular and functional correlates. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 43C, 168–184. Marsden, W. N. (2012). Synaptic plasticity in depression: Molecular, cellular and functional correlates. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 43C, 168–184.
go back to reference McDonough, J. H, Jr, & Shih, T. M. (1997). Neuropharmacological mechanisms of nerve agent-induced seizure and neuropathology. Neuroscience and Biobehavioral Reviews, 21, 559–579.PubMed McDonough, J. H, Jr, & Shih, T. M. (1997). Neuropharmacological mechanisms of nerve agent-induced seizure and neuropathology. Neuroscience and Biobehavioral Reviews, 21, 559–579.PubMed
go back to reference McDonough, J. H, Jr, Smith, R. F., & Smith, C. D. (1986). Behavioral correlates of soman-induced neuropathology: Deficits in DRL acquisition. Neurobehavioral Toxicology and Teratology, 8, 179–187.PubMed McDonough, J. H, Jr, Smith, R. F., & Smith, C. D. (1986). Behavioral correlates of soman-induced neuropathology: Deficits in DRL acquisition. Neurobehavioral Toxicology and Teratology, 8, 179–187.PubMed
go back to reference McDonough, J. H, Jr, Dochterman, L. W., Smith, C. D., & Shih, T. M. (1995). Protection against nerve agent-induced neuropathology, but not cardiac pathology, is associated with the anticonvulsant action of drug treatment. Neurotoxicology, 16, 123–132.PubMed McDonough, J. H, Jr, Dochterman, L. W., Smith, C. D., & Shih, T. M. (1995). Protection against nerve agent-induced neuropathology, but not cardiac pathology, is associated with the anticonvulsant action of drug treatment. Neurotoxicology, 16, 123–132.PubMed
go back to reference Merz, K., Herold, S., & Lie, D. C. (2011). CREB in adult neurogenesis–master and partner in the development of adult-born neurons? The European Journal of Neuroscience, 33, 1078–1086.PubMed Merz, K., Herold, S., & Lie, D. C. (2011). CREB in adult neurogenesis–master and partner in the development of adult-born neurons? The European Journal of Neuroscience, 33, 1078–1086.PubMed
go back to reference Miyaki, K., Nishiwaki, Y., Maekawa, K., Ogawa, Y., Asukai, N., et al. (2005). Effects of sarin on the nervous system of subway workers seven years after the Tokyo subway sarin attack. Journal of Occupational Health, 47, 299–304.PubMed Miyaki, K., Nishiwaki, Y., Maekawa, K., Ogawa, Y., Asukai, N., et al. (2005). Effects of sarin on the nervous system of subway workers seven years after the Tokyo subway sarin attack. Journal of Occupational Health, 47, 299–304.PubMed
go back to reference Moffett, M. C., Schultz, M. K., Schwartz, J. E., Stone, M. F., & Lumley, L. A. (2011). Impaired auditory and contextual fear conditioning in soman-exposed rats. Pharmacology, Biochemistry and Behavior, 98, 120–129.PubMed Moffett, M. C., Schultz, M. K., Schwartz, J. E., Stone, M. F., & Lumley, L. A. (2011). Impaired auditory and contextual fear conditioning in soman-exposed rats. Pharmacology, Biochemistry and Behavior, 98, 120–129.PubMed
go back to reference Nawa, H., Carnahan, J., & Gall, C. (1995). BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: Partial disagreement with mRNA levels. The European Journal of Neuroscience, 7, 1527–1535.PubMed Nawa, H., Carnahan, J., & Gall, C. (1995). BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: Partial disagreement with mRNA levels. The European Journal of Neuroscience, 7, 1527–1535.PubMed
go back to reference Oh, S. B., Park, H. R., Jang, Y. J., Choi, S. Y., Son, T. G., & Lee, J. (2013). Baicalein attenuates impaired hippocampal neurogenesis and the neurocognitive deficits induced by gamma-ray radiation. British Journal of Pharmacology, 168, 421–431.PubMedCentralPubMed Oh, S. B., Park, H. R., Jang, Y. J., Choi, S. Y., Son, T. G., & Lee, J. (2013). Baicalein attenuates impaired hippocampal neurogenesis and the neurocognitive deficits induced by gamma-ray radiation. British Journal of Pharmacology, 168, 421–431.PubMedCentralPubMed
go back to reference Ohbu, S., Yamashina, A., Takasu, N., Yamaguchi, T., Murai, T., et al. (1997). Sarin poisoning on Tokyo subway. Southern Medical Journal, 90, 587–593.PubMed Ohbu, S., Yamashina, A., Takasu, N., Yamaguchi, T., Murai, T., et al. (1997). Sarin poisoning on Tokyo subway. Southern Medical Journal, 90, 587–593.PubMed
go back to reference Otaegi, G., Yusta-Boyo, M. J., Vergano-Vera, E., Mendez-Gomez, H. R., Carrera, A. C., et al. (2006). Modulation of the PI 3-kinase-Akt signalling pathway by IGF-I and PTEN regulates the differentiation of neural stem/precursor cells. Journal of Cell Science, 119, 2739–2748.PubMed Otaegi, G., Yusta-Boyo, M. J., Vergano-Vera, E., Mendez-Gomez, H. R., Carrera, A. C., et al. (2006). Modulation of the PI 3-kinase-Akt signalling pathway by IGF-I and PTEN regulates the differentiation of neural stem/precursor cells. Journal of Cell Science, 119, 2739–2748.PubMed
go back to reference Paliouras, G. N., Hamilton, L. K., Aumont, A., Joppe, S. E., Barnabe-Heider, F., & Fernandes, K. J. (2012). Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain. The Journal of Neuroscience, 32, 15012–15026.PubMed Paliouras, G. N., Hamilton, L. K., Aumont, A., Joppe, S. E., Barnabe-Heider, F., & Fernandes, K. J. (2012). Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain. The Journal of Neuroscience, 32, 15012–15026.PubMed
go back to reference Pan, H., Hu, X. Z., Jacobowitz, D. M., Chen, C., McDonough, J., et al. (2012a). Alpha-linolenic acid is a potent neuroprotective agent against soman-induced neuropathology. Neurotoxicology, 33, 1219–1229.PubMed Pan, H., Hu, X. Z., Jacobowitz, D. M., Chen, C., McDonough, J., et al. (2012a). Alpha-linolenic acid is a potent neuroprotective agent against soman-induced neuropathology. Neurotoxicology, 33, 1219–1229.PubMed
go back to reference Pan, Y. W., Chan, G. C., Kuo, C. T., Storm, D. R., & Xia, Z. (2012b). Inhibition of adult neurogenesis by inducible and targeted deletion of ERK5 mitogen-activated protein kinase specifically in adult neurogenic regions impairs contextual fear extinction and remote fear memory. The Journal of Neuroscience, 32, 6444–6455.PubMedCentralPubMed Pan, Y. W., Chan, G. C., Kuo, C. T., Storm, D. R., & Xia, Z. (2012b). Inhibition of adult neurogenesis by inducible and targeted deletion of ERK5 mitogen-activated protein kinase specifically in adult neurogenic regions impairs contextual fear extinction and remote fear memory. The Journal of Neuroscience, 32, 6444–6455.PubMedCentralPubMed
go back to reference Paradiso, B., Zucchini, S., Su, T., Bovolenta, R., Berto, E., et al. (2011). Localized overexpression of FGF-2 and BDNF in hippocampus reduces mossy fiber sprouting and spontaneous seizures up to 4 weeks after pilocarpine-induced status epilepticus. Epilepsia, 52, 572–578.PubMed Paradiso, B., Zucchini, S., Su, T., Bovolenta, R., Berto, E., et al. (2011). Localized overexpression of FGF-2 and BDNF in hippocampus reduces mossy fiber sprouting and spontaneous seizures up to 4 weeks after pilocarpine-induced status epilepticus. Epilepsia, 52, 572–578.PubMed
go back to reference Parent, J. M. (2008). Persistent hippocampal neurogenesis and epilepsy. Epilepsia, 49(Suppl 5), 1–2.PubMed Parent, J. M. (2008). Persistent hippocampal neurogenesis and epilepsy. Epilepsia, 49(Suppl 5), 1–2.PubMed
go back to reference Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., & Lowenstein, D. H. (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. The Journal of Neuroscience, 17, 3727–3738.PubMed Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., & Lowenstein, D. H. (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. The Journal of Neuroscience, 17, 3727–3738.PubMed
go back to reference Philippens, I. H., Melchers, B. P., de Groot, D. M., & Wolthuis, O. L. (1992). Behavioral performance, brain histology, and EEG sequela after immediate combined atropine/diazepam treatment of soman-intoxicated rats. Pharmacology, Biochemistry and Behavior, 42, 711–719.PubMed Philippens, I. H., Melchers, B. P., de Groot, D. M., & Wolthuis, O. L. (1992). Behavioral performance, brain histology, and EEG sequela after immediate combined atropine/diazepam treatment of soman-intoxicated rats. Pharmacology, Biochemistry and Behavior, 42, 711–719.PubMed
go back to reference Platel, J. C., Stamboulian, S., Nguyen, I., & Bordey, A. (2010). Neurotransmitter signaling in postnatal neurogenesis: The first leg. Brain Research Reviews, 63, 60–71.PubMedCentralPubMed Platel, J. C., Stamboulian, S., Nguyen, I., & Bordey, A. (2010). Neurotransmitter signaling in postnatal neurogenesis: The first leg. Brain Research Reviews, 63, 60–71.PubMedCentralPubMed
go back to reference Raman, L., Kong, X., & Kernie, S. G. (2013). Pharmacological inhibition of the mTOR pathway impairs hippocampal development in mice. Neuroscience Letters, 541, 9–14.PubMed Raman, L., Kong, X., & Kernie, S. G. (2013). Pharmacological inhibition of the mTOR pathway impairs hippocampal development in mice. Neuroscience Letters, 541, 9–14.PubMed
go back to reference Rao, M. S., Hattiangady, B., & Shetty, A. K. (2006). The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell, 5, 545–558.PubMed Rao, M. S., Hattiangady, B., & Shetty, A. K. (2006). The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell, 5, 545–558.PubMed
go back to reference Raveh, L., Chapman, S., Cohen, G., Alkalay, D., Gilat, E., et al. (1999). The involvement of the NMDA receptor complex in the protective effect of anticholinergic drugs against soman poisoning. Neurotoxicology, 20, 551–559.PubMed Raveh, L., Chapman, S., Cohen, G., Alkalay, D., Gilat, E., et al. (1999). The involvement of the NMDA receptor complex in the protective effect of anticholinergic drugs against soman poisoning. Neurotoxicology, 20, 551–559.PubMed
go back to reference Reibel, S., Depaulis, A., & Larmet, Y. (2001). BDNF and epilepsy—the bad could turn out to be good. Trends in Neurosciences, 24, 318–319.PubMed Reibel, S., Depaulis, A., & Larmet, Y. (2001). BDNF and epilepsy—the bad could turn out to be good. Trends in Neurosciences, 24, 318–319.PubMed
go back to reference Rogers, M. A., Yamasue, H., Abe, O., Yamada, H., Ohtani, T., et al. (2009). Smaller amygdala volume and reduced anterior cingulate gray matter density associated with history of post-traumatic stress disorder. Psychiatry Research, 174, 210–216.PubMed Rogers, M. A., Yamasue, H., Abe, O., Yamada, H., Ohtani, T., et al. (2009). Smaller amygdala volume and reduced anterior cingulate gray matter density associated with history of post-traumatic stress disorder. Psychiatry Research, 174, 210–216.PubMed
go back to reference Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., et al. (2006). Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. The European journal of Neuroscience, 24, 1850–1856.PubMed Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., et al. (2006). Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. The European journal of Neuroscience, 24, 1850–1856.PubMed
go back to reference Rudge, J. S., Pasnikowski, E. M., Holst, P., & Lindsay, R. M. (1995). Changes in neurotrophic factor expression and receptor activation following exposure of hippocampal neuron/astrocyte cocultures to kainic acid. The Journal of Neuroscience, 15, 6856–6867.PubMed Rudge, J. S., Pasnikowski, E. M., Holst, P., & Lindsay, R. M. (1995). Changes in neurotrophic factor expression and receptor activation following exposure of hippocampal neuron/astrocyte cocultures to kainic acid. The Journal of Neuroscience, 15, 6856–6867.PubMed
go back to reference Rudge, J. S., Mather, P. E., Pasnikowski, E. M., Cai, N., Corcoran, T., et al. (1998). Endogenous BDNF protein is increased in adult rat hippocampus after a kainic acid induced excitotoxic insult but exogenous BDNF is not neuroprotective. Experimental Neurology, 149, 398–410.PubMed Rudge, J. S., Mather, P. E., Pasnikowski, E. M., Cai, N., Corcoran, T., et al. (1998). Endogenous BDNF protein is increased in adult rat hippocampus after a kainic acid induced excitotoxic insult but exogenous BDNF is not neuroprotective. Experimental Neurology, 149, 398–410.PubMed
go back to reference Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., et al. (2003). Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. The Journal of Neuroscience, 23, 349–357.PubMed Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., et al. (2003). Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. The Journal of Neuroscience, 23, 349–357.PubMed
go back to reference Sairanen, M., Lucas, G., Ernfors, P., Castren, M., & Castren, E. (2005). Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. The Journal of Neuroscience, 25, 1089–1094.PubMed Sairanen, M., Lucas, G., Ernfors, P., Castren, M., & Castren, E. (2005). Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. The Journal of Neuroscience, 25, 1089–1094.PubMed
go back to reference Saxe, M. D., Battaglia, F., Wang, J. W., Malleret, G., David, D. J., et al. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America, 103, 17501–17506.PubMedCentralPubMed Saxe, M. D., Battaglia, F., Wang, J. W., Malleret, G., David, D. J., et al. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America, 103, 17501–17506.PubMedCentralPubMed
go back to reference Shih, T. M., Koviak, T. A., & Capacio, B. R. (1991). Anticonvulsants for poisoning by the organophosphorus compound soman: Pharmacological mechanisms. Neuroscience and Biobehavioral Reviews, 15, 349–362.PubMed Shih, T. M., Koviak, T. A., & Capacio, B. R. (1991). Anticonvulsants for poisoning by the organophosphorus compound soman: Pharmacological mechanisms. Neuroscience and Biobehavioral Reviews, 15, 349–362.PubMed
go back to reference Shih, T. M., Skovira, J. W., O’Donnell, J. C., & McDonough, J. H. (2010). In vivo reactivation by oximes of inhibited blood, brain and peripheral tissue cholinesterase activity following exposure to nerve agents in guinea pigs. Chemico-Biological Interactions, 187, 207–214.PubMed Shih, T. M., Skovira, J. W., O’Donnell, J. C., & McDonough, J. H. (2010). In vivo reactivation by oximes of inhibited blood, brain and peripheral tissue cholinesterase activity following exposure to nerve agents in guinea pigs. Chemico-Biological Interactions, 187, 207–214.PubMed
go back to reference Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., & Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus, 12, 578–584.PubMedCentralPubMed Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., & Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus, 12, 578–584.PubMedCentralPubMed
go back to reference Sinor, A. D., & Lillien, L. (2004). Akt-1 expression level regulates CNS precursors. The Journal of Neuroscience, 24, 8531–8541.PubMed Sinor, A. D., & Lillien, L. (2004). Akt-1 expression level regulates CNS precursors. The Journal of Neuroscience, 24, 8531–8541.PubMed
go back to reference Slipczuk, L., Bekinschtein, P., Katche, C., Cammarota, M., Izquierdo, I., & Medina, J. H. (2009). BDNF activates mTOR to regulate GluR1 expression required for memory formation. PLoS One, 4, e6007.PubMedCentralPubMed Slipczuk, L., Bekinschtein, P., Katche, C., Cammarota, M., Izquierdo, I., & Medina, J. H. (2009). BDNF activates mTOR to regulate GluR1 expression required for memory formation. PLoS One, 4, e6007.PubMedCentralPubMed
go back to reference Smith, E. D., Prieto, G. A., Tong, L., Sears-Kraxberger, I., Rice, J. D., et al. (2014). Rapamycin and interleukin-1beta impair brain-derived neurotrophic factor-dependent neuron survival by modulating autophagy. The Journal of Biological Chemistry, 289, 20615–20629.PubMedCentralPubMed Smith, E. D., Prieto, G. A., Tong, L., Sears-Kraxberger, I., Rice, J. D., et al. (2014). Rapamycin and interleukin-1beta impair brain-derived neurotrophic factor-dependent neuron survival by modulating autophagy. The Journal of Biological Chemistry, 289, 20615–20629.PubMedCentralPubMed
go back to reference Snyder, J. S., Hong, N. S., McDonald, R. J., & Wojtowicz, J. M. (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience, 130, 843–852.PubMed Snyder, J. S., Hong, N. S., McDonald, R. J., & Wojtowicz, J. M. (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience, 130, 843–852.PubMed
go back to reference Solberg, Y., & Belkin, M. (1997). The role of excitotoxicity in organophosphorous nerve agents central poisoning. Trends in Pharmacological Sciences, 18, 183–185.PubMed Solberg, Y., & Belkin, M. (1997). The role of excitotoxicity in organophosphorous nerve agents central poisoning. Trends in Pharmacological Sciences, 18, 183–185.PubMed
go back to reference Soppet, D., Escandon, E., Maragos, J., Middlemas, D. S., Reid, S. W., et al. (1991). The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell, 65, 895–903.PubMed Soppet, D., Escandon, E., Maragos, J., Middlemas, D. S., Reid, S. W., et al. (1991). The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell, 65, 895–903.PubMed
go back to reference Stubley-Weatherly, L., Harding, J. W., & Wright, J. W. (1996). Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Research, 716, 29–38.PubMed Stubley-Weatherly, L., Harding, J. W., & Wright, J. W. (1996). Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Research, 716, 29–38.PubMed
go back to reference Suarez-Pereira, I., Canals, S., & Carrion, A. M. (2014). Adult newborn neurons are involved in learning acquisition and long-term memory formation: The distinct demands on temporal neurogenesis of different cognitive tasks. Hippocampus, 25, 51–61.PubMed Suarez-Pereira, I., Canals, S., & Carrion, A. M. (2014). Adult newborn neurons are involved in learning acquisition and long-term memory formation: The distinct demands on temporal neurogenesis of different cognitive tasks. Hippocampus, 25, 51–61.PubMed
go back to reference Swiech, L., Perycz, M., Malik, A., & Jaworski, J. (2008). Role of mTOR in physiology and pathology of the nervous system. Biochimica et Biophysica Acta, 1784, 116–132.PubMed Swiech, L., Perycz, M., Malik, A., & Jaworski, J. (2008). Role of mTOR in physiology and pathology of the nervous system. Biochimica et Biophysica Acta, 1784, 116–132.PubMed
go back to reference Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., et al. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nature Neuroscience, 11, 901–907.PubMedCentralPubMed Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., et al. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nature Neuroscience, 11, 901–907.PubMedCentralPubMed
go back to reference Toomey, R., Alpern, R., Vasterling, J. J., Baker, D. G., Reda, D. J., et al. (2009). Neuropsychological functioning of U.S. Gulf War veterans 10 years after the war. Journal of the International Neuropsychological Society, 15, 717–729.PubMed Toomey, R., Alpern, R., Vasterling, J. J., Baker, D. G., Reda, D. J., et al. (2009). Neuropsychological functioning of U.S. Gulf War veterans 10 years after the war. Journal of the International Neuropsychological Society, 15, 717–729.PubMed
go back to reference van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature, 415, 1030–1034.PubMed van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature, 415, 1030–1034.PubMed
go back to reference Wullschleger, S., Loewith, R., & Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell, 124, 471–484.PubMed Wullschleger, S., Loewith, R., & Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell, 124, 471–484.PubMed
go back to reference Yamada, T., Uchida, H., & Ichikawa, A. (1983). Detection of learning impairment in offspring in reproduction tests. Jikken dobutsu. Experimental Animals, 32, 107–113.PubMed Yamada, T., Uchida, H., & Ichikawa, A. (1983). Detection of learning impairment in offspring in reproduction tests. Jikken dobutsu. Experimental Animals, 32, 107–113.PubMed
go back to reference Yamasue, H., Kasai, K., Iwanami, A., Ohtani, T., Yamada, H., et al. (2003). Voxel-based analysis of MRI reveals anterior cingulate gray-matter volume reduction in posttraumatic stress disorder due to terrorism. Proceedings of the National Academy of Sciences of the United States of America, 100, 9039–9043.PubMedCentralPubMed Yamasue, H., Kasai, K., Iwanami, A., Ohtani, T., Yamada, H., et al. (2003). Voxel-based analysis of MRI reveals anterior cingulate gray-matter volume reduction in posttraumatic stress disorder due to terrorism. Proceedings of the National Academy of Sciences of the United States of America, 100, 9039–9043.PubMedCentralPubMed
go back to reference Yang, W. M., Shim, K. J., Choi, M. J., Park, S. Y., Choi, B. J., et al. (2008). Novel effects of Nelumbo nucifera rhizome extract on memory and neurogenesis in the dentate gyrus of the rat hippocampus. Neuroscience Letters, 443, 104–107.PubMed Yang, W. M., Shim, K. J., Choi, M. J., Park, S. Y., Choi, B. J., et al. (2008). Novel effects of Nelumbo nucifera rhizome extract on memory and neurogenesis in the dentate gyrus of the rat hippocampus. Neuroscience Letters, 443, 104–107.PubMed
go back to reference Zeng, L. H., Xu, L., Gutmann, D. H., & Wong, M. (2008). Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Annals of neurology, 63, 444–453.PubMedCentralPubMed Zeng, L. H., Xu, L., Gutmann, D. H., & Wong, M. (2008). Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Annals of neurology, 63, 444–453.PubMedCentralPubMed
go back to reference Zhao, C., Deng, W., & Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132, 645–660.PubMed Zhao, C., Deng, W., & Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132, 645–660.PubMed
Metadata
Title
Alpha-Linolenic Acid-Induced Increase in Neurogenesis is a Key Factor in the Improvement in the Passive Avoidance Task After Soman Exposure
Authors
Tetsade CB Piermartiri
Hongna Pan
Jun Chen
John McDonough
Neil Grunberg
James P. Apland
Ann M. Marini
Publication date
01-09-2015
Publisher
Springer US
Published in
NeuroMolecular Medicine / Issue 3/2015
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI
https://doi.org/10.1007/s12017-015-8353-y

Other articles of this Issue 3/2015

NeuroMolecular Medicine 3/2015 Go to the issue