JBBS> Vol.2 No.2, May 2012

Influence of Iron Deficiency on Olfactory Behavior in Weanling Rats

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ABSTRACT

Chronically high occupational exposure to airborne metals like iron can impair olfactory function, but little is known about how low iron status modifies olfactory behavior. To investigate the influence of body iron status, weanling rats were fed a diet with low iron content (4 - 7 ppm) to induce iron deficiency anemia and olfactory behavior was compared to control rats fed an isocaloric diet sufficient in iron (210 - 220 ppm). Iron-deficient rats had prolonged exploratory time for attractive odorants in behavioral olfactory habituation/dishabituation tests, olfactory preference tests and olfactory sensitivity tests compared with control rats. No significant differences were observed for aversive odorants between the two groups. These findings suggest that iron-dependent functions may be involved in controlling and processing of olfactory signal transduction via self and lateral inhibition such that odorant signal remains stronger for longer times prolonging exploratory activity on attractive odorants in the behavioral tests. These findings establish that iron deficiency can modify olfactory behavior.

Cite this paper

V. Ruvin Kumara and M. Wessling-Resnick, "Influence of Iron Deficiency on Olfactory Behavior in Weanling Rats," Journal of Behavioral and Brain Science, Vol. 2 No. 2, 2012, pp. 167-175. doi: 10.4236/jbbs.2012.22020.

References

[1] M. B. Antunes, R. Bowler and R. L. Doty, “San Francisco/Oakland Bay Bridge Welder Study: Olfactory Function,” Neurology, Vol. 69, No. 12, 2007, pp. 1278-1284. doi:10.1212/01.wnl.0000276988.50742.5e
[2] R. L. Doty, M. Riklan, D. A. Deems, C. Reynolds and S. Stellar, “The Olfactory and Cognitive Deficits of Parkinson’s Disease: Evidence for Independence,” Annals of Neurology, Vol. 25, No. 2, 1989, pp 166-71. doi:10.1002/ana.410250210
[3] T. Baba, A. Takeda, A. Kikuchi, Y. Nishio, Y. Hosokai, K. Hirayama, T. Hasegawa, N. Sugeno, K. Suzuki, E. Mori, S. Takahashi, H. Fukuda and Y. Itoyama, “Association of Olfactory Dysfunction and Brain. Metabolism in Parkinson’s Disease,” Movement Disorders, Vol. 26, No. 4, 2011, pp. 621-628. doi: 10.1002/mds.23602
[4] M. Fusetti, A. B. Fioretti, F. Silvagni, M. Simaskou, P. Sucapane, S. Necozione and A. Eibenstein, “Smell and Preclinical Alzheimer Disease: Study of 29 Patients with Amnesic Mild Cognitive Impairment,” Journal of Otolaryngology Head and Neck Surgery, Vol. 39, No. 2, 2010, pp. 175-181. doi:10.2310/7070.2009.090046
[5] S. Forster, A. Vaitl, S. J. Teipel, I. Yakushev, M. Mustafa, C. la Fougere, A. Rominger, P. Cumming, P. Bartenstein, H. Hampel, T. Hummel, K. Buerger, W. Hundt and S. Steinbach, “Functional Representation of Olfactory Impairment in Early Alzheimer’s Disease,” Journal of Alzheimers Disease, Vol. 22, No. 2, 2010, pp. 581-591. doi:10.3233/JAD-2010-091549
[6] T. Kovacs, “Mechanisms of Olfactory Dysfunction in Aging and Neurodegenerative Disorders,” Ageing Research Reviews, Vol. 3, No. 2, 2004, pp. 215-232. doi:10.1016/j.arr.2003.10.003
[7] H. J. Westervelt, J. Carvalho and K. Duff, “Presentation of Alzheimer’s Disease in Patients with and without Olfactory Deficits,” Archives of Clinical Neuropsychology, Vol. 22, No.1, 2007, pp. 117-122. doi:10.1016/j.acn.2006.11.005
[8] J. F. Morley and J. E. Duda, “Olfaction as a Biomarker in Parkinson’s Disease,” Biomark Medicine, Vol. 4, No. 5, 2010, pp. 661-670. doi:10.2217/BMM.10.95
[9] R. I. Mesholam, P. J. Moberg, R. N. Mahr and R. L. Doty, “Olfaction in Neurodegenerative Disease: A Meta-Analysis of Olfactory Functioning in Alzheimer’s and Parkinson’s diseases,” Archives of Neurology, Vol. 55, No. 1, 1998, pp. 84-90. doi:10.1001/archneur.55.1.84
[10] M. W. Albers, M. H. Tabert and D. P. Devanand, “Olfactory Dysfunction as a Predictor of Neurodegenerative Disease,” Current Neurology and Neuroscience Reports, Vol. 6, No. 5, 2006, pp. 379-386. doi:10.1007/s11910-996-0018-7
[11] R. L. Doty, “The Olfactory Vector Hypothesis of Neurodegenerative Disease: Is It Viable?” Annals of Neurology, Vol. 63, No. 1, 2008, pp. 7-15. doi:10.1002/ana.21327
[12] J. Wang, P. J. Eslinger, R. L. Doty, E. K. Zimmerman, R. Grunfeld, X. Sun, M. D. Meadowcroft, J. R. Connor, J. L. Price, M. B. Smith and Q. X. Yang, “Olfactory Deficit Detected by fMRI in Early Alzheimer’s Disease,” Brain Research, Vol. 1357, 2010, pp. 184-194. doi:10.1016/j.brainres.2010.08.018
[13] M. Schrag, C. Mueller, U. Oyoyo, M. A. Smith and W. M. Kirsch, “Iron Zinc and Copper in the Alzheimer’s Disease Brain: A Quantitative Meta-Analysis. Some Insight on the Influence of Citation Bias on Scientific Opinion,” Progress in Neurobiology, Vol. 94, No. 3, 2011, pp. 296-306. doi:10.1016/j.pneurobio.2011.05.001
[14] G. A. Salvador, R. M. Uranga and N. M. Giusto, “Iron and Mechanisms of Neurotoxicity,” International Journal of Alzheimers Disease, Vol. 2011, 2010, Article ID 720658. doi: 10.4061/2011/720658
[15] W. Y. Ong and A. A. Farooqui, “Iron, Neuroinflammation, and Alzheimer’s Disease,” Journal of Alzheimers Disease, Vol. 8, No. 2, 2005, pp. 183-200, discussion 209-115.
[16] C. Quintana, S. Bellefqih, J. Y. Laval, J. L. Guerquin-Kern, T. D. Wu, J. Avila, I. Ferrer, R. Arranz and C. Patino, “Study of the Localization of Iron, Ferritin, and Hemosiderin in Alzheimer’s Disease Hippocampus by Analytical Microscopy at the Subcellular Level,” Journal of Structural Biology, Vol. 153, No. 1, 2006, pp. 42-54. doi:10.1016/j.jsb.2005.11.001
[17] T. A. Rouault, “Systemic Iron Metabolism: A Review and Implications for Brain Iron Metabolism,” Pediatric Neurology, Vol. 25, No .2, 2001, pp. 130-137. doi:10.1016/S0887-8994(01)00260-0
[18] B. N. Johnson, J. D. Mainland and N. Sobel, “Rapid Olfactory Processing Implicates Subcortical Control of an Olfactomotor System,” Journal of Neurophysiology, Vol. 90, No. 2, 2003, pp. 1084-1094. doi:10.1152/jn.00115.2003
[19] J. Porter, B. Craven, R. M. Khan, S. J. Chang, I. Kang, B. Judkewitz, J. Volpe, G. Settles and N. Sobel, “Mechanisms of Scent-Tracking in Humans,” Nature Neuroscience, Vol. 10, No. 1, 2007, pp. 27-29. doi:10.1038/nn0207-263d
[20] S. L. Youngentob, M. M. Mozell, P. R. Sheehe and D. E. Hornung, “A Quantitative Analysis of Sniffing Strategies in Rats Performing Odor Detection Tasks,” Physiology & Behavior, Vol. 41, No. 1, 1987, pp. 59-69. doi:10.1016/0031-9384(87)90131-4
[21] K. G. Sorwell, D. W. Wesson and M. J. Baum, “Sexually Dimorphic Enhancement by Estradiol of Male Urinary Odor Detection Thresholds in Mice,” Behavioral Neuroscience, Vol. 122, No. 4, 2008, pp. 788-793. doi:10.1037/0735-7044.122.4.788
[22] D. W. Wesson, T. N. Donahou, M. O. Johnson and M. Wachowiak, “Sniffing Behavior of Mice During Performance in Odor-Guided Tasks,” Chemical Senses, Vol. 33, No. 7, 2008, pp. 581-596. doi:10.1093/chemse/bjn029
[23] M. Yang and J. N. Crawley, “Simple Behavioral Assessment of Mouse Olfaction,” Current Protocols in Neuroscience, Chapter 8, 2009, Unit 8.24. doi:10.1002/0471142301.ns0824s48
[24] J. D. Brain, E. Heilig, T. C. Donaghey, M. D. Knutson, M. Wessling-Resnick and R. M. Molina, “Effects of Iron Status on Transpulmonary Transport and Tissue Distribution of Mn and Fe,” American Journal of Respiratory Cell and Molecular Biology, Vol. 34, No. 3, 2006, pp. 330-337. doi:10.1165/rcmb.2005-0101OC
[25] M. Kadohisa and D. A. Wilson, “Olfactory Cortical Adaptation Facilitates Detection of Odors Against Background,” Journal of Neurophysiology, Vol. 95, No. 3, 2006, pp. 1888-1896. doi:10.1152/jn.00812.2005
[26] D. Chaudhury, L. Manella, A. Arellanos, O. Escanilla, T. A. Cleland and C. Linster, “Olfactory Bulb Habituation to Odor Stimuli,” Behavioral Neuroscience, Vol. 124, No. 4, 2010, pp. 490-499. doi:10.1037/a0020293
[27] K. Kobayakawa, R. Kobayakawa, H. Matsumoto, Y. Oka, T. Imai, M. Ikawa, M. Okabe, T. Ikeda, S. Itohara, T. Kikusui, K. Mori and H. Sakano, “Innate versus Learned Odour Processing in the Mouse Olfactory Bulb,” Nature, Vol. 450, No. 7169, 2007, pp. 503-508. doi:10.1038/nature06281
[28] R. M. Witt, M. M. Galligan, J. R. Despinoy and R. Segal, “Olfactory Behavioral Testing in the Adult Mouse,” Journal of Visualized Experiment, Vol. 23, 2009, p. 949. doi:10.3791/949
[29] T. Yabumoto, F. Takanashi, Y. Kirino and S. Watanabe, “Nitric Oxide Is Involved in Appetitive but Not Aversive Olfactory Learning in the Land Mollusk Limax Valentianus,” Learning & Memory, Vol. 15, No. 4, 2008, pp. 229-232. doi:10.1101/lm.936508
[30] A. C. Keene and S. Waddell, “Drosophila Memory: Dopamine Signals Punishment?” Current Biology, Vol. 15, No. 22, 2005, pp. R932-934. doi:10.1016/j.cub.2005.11.040
[31] S. Unoki, Y. Matsumoto and M. Mizunami, “Participation of Octopaminergic Reward System and Dopaminergic Punishment System in Insect Olfactory Learning Revealed by Pharmacological Study,” European Journal of Neuroscience, Vol. 22, No. 6, 2005, pp. 1409-1416. doi:10.1111/j.1460-9568.2005.04318.x
[32] V. Vergoz, E. Roussel, J. C. Sandoz and M. Giurfa, “Aversive Learning in Honeybees Revealed by the Olfactory Conditioning of the Sting Extension Reflex,” PLoS One, Vol. 2, No. 23, 2007, pp. e288. doi:10.1371/journal.pone.0000288
[33] D. Brunert, S. Kurtenbach, S. Isik, H. Benecke, G. Gisselmann, W. Schuhmann, H. Hatt and C. H. Wetzel, “Odorant-Dependent Generation of Nitric Oxide in Mammalian Olfactory Sensory Neurons,” PLoS One, Vol. 4, No. 5, 2009, p. e5499. doi:10.1371/journal.pone.0005499
[34] M. Doengi, D. Hirnet, P. Coulon, H.C. Pape, J.W. Deitmer and C. Lohr, “GABA Uptake-Dependent Ca(2+) Signaling in Developing Olfactory Bulb Astrocytes,” Proceedings of the National Academy of Sciences USA, Vol. 106, No. 41, 2009, pp. 17570-17575. doi:10.1073/pnas.0809513106
[35] A. Larkin, S. Karak, R. Priya, A. Das, C. Ayyub, K. Ito, V. Rodrigues and M. Ramaswami, “Central Synaptic Mechanisms Underlie Short-Term Olfactory Habituation in Drosophila Larvae,” Learning & Memory, Vol. 17, No. 12, 2010, pp. 645-653. doi:10.1101/lm.1839010
[36] S. Das, M. K. Sadanandappa, A. Dervan, A. Larkin, J. A. Lee, I. P. Sudhakaran, R. Priya, R. Heidari, E. E. Holohan, A. Pimentel, A. Gandhi, K. Ito, S. Sanyal, J. W. Wang, V. Rodrigues and M. Ramaswami, “Plasticity of Local Gabaergic Interneurons Drives Olfactory Habituation,” Proceedings of the National Academy of Sciences USA, Vol. 108, No. 36, 2011, pp, E646-654. doi:10.1073/pnas.1106411108
[37] R. Matsuo and E. Ito, “A Novel Nitric Oxide Synthase Expressed Specifically in the Olfactory Center,” Biochemical and Biophysical Research Communications, Vol. 386, No. 4, 2009, pp. 724-728. doi:10.1016/j.bbrc.2009.06.112
[38] B. Samama and N. Boehm, “Inhibition of Nitric Oxide Synthase Impairs Early Olfactory Associative Learning in Newborn Rats,” Neurobiology of Learn Memory, Vol. 71, No. 2, 1999, pp. 219-231. doi:10.1006/nlme.1998.3869
[39] M. R. Poston, M. S. Bailey, R. Schwarcz and M. T. Shipley, “Differential Complementary Localization of Metabolic Enzymes for Quinolinic Acid in Olfactory Bulb Astrocytes,” The Journal of Comparative Neurology, Vol. 311, No. 3, 1991, pp. 367-374. doi:10.1002/cne.903110307
[40] J. C. Brown Ⅲ, H. W. Tse, D. A. Skifter, J. M. Christie, V. J. Andaloro, M. C. Kemp, J. C. Watkins, D. E. Jane and D. T. Monaghan, “[3H]Homoquinolinate Binds to a Subpopulation of NMDA Receptors and to a Novel Binding Site,” Journal of Neurochemistry, Vol. 71, No. 4, 1998, pp. 1464-1470. doi:10.1046/j.1471-4159.1998.71041464.x
[41] M. Wolfensberger, U. Amsler, M. Cuenod, A.C. Foster, W. O. Whetsell Jr. and R. Schwarcz, “Identification of Quinolinic Acid in Rat and Human Brain Tissue,” Neuroscience Letters, Vol. 41, No. 3, 1983, pp. 247-252. doi:10.1016/0304-3940(83)90458-5
[42] T. W. Stone, “Neuropharmacology of Quinolinic and Kynurenic Acids,” Pharmacological Reviews, Vol. 45, No. 3, 1993, pp. 309-379.
[43] G. J. Guillemin, K. M. Cullen, C. K. Lim, G. A. Smythe, B. Garner, V. Kapoor, O. Takikawa and B. J. Brew, “Characterization of the Kynurenine Pathway in Human Neurons,” Journal of Neuroscience, Vol. 27, No. 47, 2007, pp. 12884-12892. doi:10.1523/JNEUROSCI.4101-07.2007
[44] G. G. Collins, J. Anson and G. A. Probett, “Excitatory and Inhibitory Effects of Dopamine on Synaptic Transmission in the Rat Olfactory Cortex Slice,” Brain Research, Vol. 333, No. 2, 1985, pp. 237-245. doi:10.1016/0006-8993(85)91577-X
[45] J. W. Cave and H. Baker, “Dopamine Systems in the Forebrain,” Advances in Experimental Medicine and Biology, Vol. 651, 2009, pp. 15-35. doi:10.1007/978-1-4419-0322-8_2
[46] M. Ennis, F. M. Zhou and K. J. Ciombor, “Dopamine D2 Receptor-Mediated Presynaptic Inhibition Olfactory Nerve Terminals,” Journal of Neurophysiology, Vol. 86, No. 6, 2001, pp. 2986-2997.
[47] D. A. Berkowicz and P. Q. Trombley, “Dopaminergic Modulation at the Olfactory Nerve Synapse,” Brain Research, Vol. 855, No. 1, 2000, pp. 90-99. doi:10.1016/S0006-8993(99)02342-2
[48] A. Y. Hsia, J. D. Vincent and P. M. Lledo. “Dopamine Depresses Synaptic Inputs into the Olfactory Bulb,” Journal of Neurophysiology, Vol. 82, No. 2, 1999, pp. 1082-1085.
[49] T. Chernova, J. R. Steinert, P. Richards, R. Mistry, R. A. Challiss, R. Jukes-Jones, K. Cain, A. G. Smith and I. D. Forsythe, “Early Failure of N-Methyl-D-Aspartate Receptors and Deficient Spine Formation Induced by Reduction of Regulatory Heme in Neurons,” Molecular Pharmacology, Vol. 79, No. 5, 2011, pp. 844-854. doi:10.1124/mol.110.069831
[50] T. Chernova, P. Nicotera and A. G. Smith, “Heme deficiency Is Associated with Senescence and Causes Suppression of N-Methyl-D-Aspartate Receptor Subunits Expression in Primary Cortical Neurons,” Molecular Pharmacology, Vol. 69, No. 3, 2006, pp. 697-705. doi:10.1124/mol.105.016675
[51] N. Mandairon, C. Stack, C. Kiselycznyk and C. Linster, “Broad Activation of the Olfactory Bulb Produces Long-Lasting Changes in Perception,” Proceedings of the National Academy of Sciences, Vol. 103, No. 36, 2006, pp. 13543-13548. doi:10.1073/pnas.0602750103
[52] N. Mandairon, C. Stack and C. Linster, “Olfactory Enrichment Improves the Recognition of Individual Components in Mixtures,” Physiology & Behavior, Vol. 89, No. 3, 2006, pp. 379-384. doi:10.1016/j.physbeh.2006.07.013
[53] N. N. Urban and B. Sakmann, “Reciprocal Intraglomerular Excitation and Intra- and Interglomerular Lateral Inhibition between Mouse Olfactory Bulb Mitral Cells,” Journal of Physiology, Vol. 542, No. 2, 2002, pp. 355-367. doi:10.1113/jphysiol.2001.013491
[54] K. Mori and S. F. Takagi, “An Intracellular Study of Dendrodendritic Inhibitory Synapses on Mitral Cells in the Rabbit Olfactory Bulb,” Journal of Physiology, Vol. 279, 1978, pp. 569-588.
[55] C. E. Jahr and R. A. Nicoll, “Dendrodendritic Inhibition: Demonstration with Intracellular Recording,” Science, Vol. 207, No. 4438, 1980, pp. 1473-1475. doi:10.1126/science.7361098
[56] M. C. Nowycky, K. Mori and G. M. Shepherd, “GABAergic Mechanisms of Dendrodendritic Synapses in Isolated Turtle Olfactory Bulb,” Journal of Neurophysiology, Vol. 46, No. 3, 1981, pp. 639-648.
[57] J. S. Isaacson and B. W. Strowbridge, “Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS,” Neuron, Vol. 20, No. 4, 1998, pp. 749-761. doi:10.1016/S0896-6273(00)81013-2

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