Olfactory Discrimination in Adult Male Rats Undernourished during the Pre- and Neonatal Period


In the neonatal rat, the olfactory system is a fundamental channel to locate and recognize the mother, to survive and develop early social behavior, and to distinguish related or unrelated members of a litter. Perinatal undernutrition in rats alters the neuronal organization and functioning of the olfactory system and its ascending relays, possibly affecting odor discrimination. In this study we compared the frequency and time spent visiting the source of urine obtained from unrelated female subjects and amyl acetate odors vs water in adult perinatally underfed rats. Each test initiated with one daily presentation during three consecutive aliquots of deionized water (10 μl) placed on a filter paper for 2 min, separated by 1-min intervals for habituation. The water presentations were followed by three exposures to an odor, all at the same dilution (either 1:1 or 1:80) for dishabituation. Control (C) and undernourished (U) subjects display similar, significant habituation/dishabituation responses, except that the U subjects showed greater increases in the frequency and duration of visits to undiluted and diluted urine and amyl acetate cues compared to the controls. These findings are similar to previous studies showing that adult rats investigate novel odors longer than the familiar ones. Thus, perinatal undernutrition appears to interfere with the foundation of the olfactory development causing long-term olfactory discrimination deficits as revealed by the increased frequency and duration of visits to the source of odors that may be relevant for social behavior.

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M. Carreon, C. Torrero, M. Regalado, L. Rubio and M. Salas, "Olfactory Discrimination in Adult Male Rats Undernourished during the Pre- and Neonatal Period," Journal of Behavioral and Brain Science, Vol. 2 No. 3, 2012, pp. 283-290. doi: 10.4236/jbbs.2012.23032.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] W. S. Small, “Notes on the Psychic Development of the Young White Rat,” American Journal of Psychology, Vol. 11, No. 1, 1899, pp. 80-100. doi:10.2307/1412730
[2] D. A. Callison and J. W. Spencer, “Effect of Chronic Undernutrition and/or Visual Deprivation upon the Visual Evoked Potential from the Developing Rat Brain,” Developmental Psychobiology, Vol. 1, No. 3, 1968, pp. 196-204. doi:10.1002/dev.420010308
[3] M. Salas, S. Schapiro and C. Guzman-Flores, “Development of Olfactory Bulb Discrimination between Maternal and Food Odors,” Physiology and Behavior, Vol. 5, No. 1, 1970, pp. 1261-1264. doi:10.1016/0031-9384(70)90037-5
[4] M. H. Teicher and E. M. Blass, “First Suckling Response of the Newborn Albino Rat: The Roles of Olfaction and Amniotic Fluid,” Science, Vol. 198, No. 4317, 1977, pp. 635-636. doi:10.1126/science.918660
[5] R. Coopersmith and L. Leon, “The Neurobiology of Early Olfactory Learning,” In: E. M. Blass, Ed., Developmental Psychobiology and Behavioral Ecology, Plenum Press, New York, 1988, pp. 283-308. doi:10.1007/978-1-4684-5421-5_8
[6] C. Raineki, A. Pickenhagen, T. L. Roth, D. M. Babstock, J. H. McLean, C. W. Harley, A. B. Lucion and R. M. Sullivan, “The Neurobiology of Infant Maternal Odor Learning,” Brazilian Journal of Medical and Biological Research, Vol. 43, No. 10, 2010, pp. 914-919. doi:10.1590/S0100-879X2010007500090
[7] C. Nyakas and E. Endroczi, “Olfaction-Guided Approaching Behavior of Infantile Pups to the Mother in a Maze Box,” Acta Physiologica Academiae Scientiarum Hungaricae, Vol. 38, No. 1, 1970, pp. 59-65.
[8] R. M. Sullivan, D. A. Wilson, R Wong, A. Correa and M. Leon, “Modified Behavioral and Olfactory Bulb Responses to Maternal Odors in Preweanling Rats,” Brain Research, Developmental Brain Research, Vol. 53, No. 2, 1990, pp. 243-247. doi:10.1016/0165-3806(90)90013-O
[9] S. Moriceau and R. M. Sullivan, “Maternal Presence Serves as a Switch between Learning Fear and Attraction in Infancy,” Nature Neuroscience, Vol. 9, No. 8, 2006, pp. 1004-1006. doi:10.1038/nn1733
[10] C. Frias, C. Torrero, M. Regalado and M Salas, “Organization of Olfactory Glomeruli in Neonatally Undernourished Rats,” Nutritional Neuroscience, Vol. 9, No. 1-2, 2006, pp. 49-55. doi:10.1080/10284150500506042
[11] C. Frias, C. Torrero, M. Regalado and M. Salas, “Development of Mitral Cells and Olfactory Bulb Layers in Neonatally Undernourished Rats,” Nutritional Neuroscience, Vol. 12, No. 3, 2009, pp. 96-104. doi:10.1179/147683009X423238
[12] M. Ruiz-Diaz, C. Torrero, M. Regalado and M. Salas, “Perinatal Undernourishment and Handling: Effects on Olfactory Discrimination in the Newborn Rat,” Nutritional Neuroscience, Vol. 13, No. 5, 2010, pp. 196-204. doi:10.1179/147683010X12611460764408
[13] B. G. Cragg, “The Development of Cortical Synapses during Starvation in the Rat,” Brain, Vol. 95, No. 1, 1972, pp. 143-150. doi:10.1093/brain/95.1.143
[14] M. Salas, “Effects of Early Undernutrition on Dendritic Spines of Cortical Pyramidal Cells in the Rat,” Developmental Neuroscience, Vol. 3, No. 3, 1980, pp. 109-117. doi:10.1159/000112384
[15] C. Escobar and M. Salas, “Neonatal Undernutrition and Amygdaloid Nuclear Complex Development: An Experimental Study in the Rat,” Experimental Neurology, Vol. 122, No. 2, 1993, pp. 311-318. doi:10.1006/exnr.1993.1130
[16] J. P. Andrade, M. D. Madeira and M. M. Paula-Barbosa, “Evidence of Reorganization in the Hippocampal Mossy Fiber Synapses of Adult Rats Rehabilitated after Prolonged Undernutrition,” Experimental Brain Research, Vol. 104, No. 2, 1995, pp. 249-261. doi:10.1007/BF00242011
[17] L. Rubio, C. Torrero, M. Regalado and M. Salas, “Alterations in the Solitary Tract Nucleus of the Rat Following Perinatal Food Restriction and Subsequent Nutritional Rehabilitation,” Nutritional Neuroscience, Vol. 7, No. 5-6, 2004, pp. 291-300. doi:10.1080/10284150400019922
[18] F. Math and J. L. Davrainville, “Electrophysiological Study on the Postnatal Development of Mitral Cell Activity in the Rat Olfactory Bulb. Influence of Undernutrition,” Brain Research, Vol. 194, No. 1, 1980, pp. 223-227. doi:10.1016/0006-8993(80)91333-5
[19] K. S. Bedi, “Effects of Undernutrition during Early Life on Granule Cell Numbers in the Rat Dentate Gyrus,” The Journal of Comparative Neurology, Vol. 311 No. 10, 1991, pp. 425-433. doi:10.1002/cne.903110311
[20] M. Salas, C. Torrero and S. Pulido, “Long-Term Alterations in the Maternal Behavior of Neonatally Undernourished Rats,” Physiology and Behavior, Vol. 33, No. 2, 1984, pp. 273-278. doi:10.1016/0031-9384(84)90111-2
[21] A. Lynch, “Postnatal Undernutrition: An Alternative method,” Developmental Psychobiology, Vol. 9, No. 1, 1976, pp. 39-48. doi:10.1002/dev.420090107
[22] L. Rosselli-Austin and J. Altman, “The Postnatal Development of the Main Olfactory Bulb of the Rat,” Journal of Developmental Physiology, Vol. 1, No. 4, 1979, pp. 295-313.
[23] K. Lydell and R. L. Doty. “Male Rat Odor Preferences for Female Urine as a Function of Sexual Experience, Urine Age, and Urine Source,” Hormones and Behavior, Vol. 3, No. 3, 1972, pp. 205-212. doi:10.1016/0018-506X(72)90033-5
[24] R. E. Brown, H. M. Schellinck and A. M. West, “The Influence of Dietary and Genetic Cues on the Ability of Rats to Discriminate between the Urinary Odors of MHC-Congenic Mice,” Physiology and Behavior, Vol. 60, No. 2, 1996, pp. 365-372. doi:10.1016/S0031-9384(96)80006-0
[25] C. Zalaquett and D. Thiessen, “The Effects of Odors from Stressed Mice on Conspecific Behavior,” Physiology and Behavior, Vol. 50, No. 1, 1991, pp. 221-227. doi:10.1016/0031-9384(91)90524-R
[26] M. J. Baum and E. B. Keverne, “Sex Difference in Attraction Thresholds for Volatile Odors from Male and Estrous Female Mouse Urine,” Hormones and Behavior, Vol. 41, No. 2, 2002, pp. 213-219. doi:10.1006/hbeh.2001.1749
[27] C. M. Khun, S. R. Butler and S. M. Schanberg, “Selective Depression of Serum Growth Hormone during Maternal Deprivation in Rat Pups,” Science, Vol. 201, No. 4360, 1978, pp. 1034-1036. doi:10.1126/science.684424
[28] C. Wimpfheimer, E. Saville, M. J. Voirol, E. Danforth Jr. and A. G. Burger, “Starvation-Induced Decreased Sensitivity of Resting Metabolic Rate to Triiodothyronine,” Science, Vol. 4412, No. 205, 1979, pp. 1272-1273. doi:10.1126/science.224460
[29] G. E. Evoniuk, C. M. Kuhn and S. M. Schanberg, “The Effect of Tactile Stimulation on Serum Growth Hormone and Tissue Ornithine Decarboxylase Activity during Maternal Deprivation in Rat Pups,” Communications in Psychopharmacology, Vol. 3, No. 5, 1979, pp. 363-370.
[30] S. M. Schanberg, G. E. Evoniuk and C. M. Kuhn, “Tactile and Nutritional Aspects of Maternal Care: Specific Regulators of Neuroendocrine Function and Cellular Development,” Proceedings of the Society for Experimental Biology and Medicine, Vol. 175, No. 2, 1984, pp. 135-146.
[31] J. M. Ketelslegers, D. Maiter, M. Maes, L. E. Underwood and J. P. Thissen, “Nutritional Regulation of the Growth Hormone and Insulin-Like Growth Factor-Binding Proteins,” Hormone Research, Vol. 45, No. 3-5, 1996, pp. 252-257. doi:10.1159/000184797
[32] B. M. Lester, R. E. Klein and S. J. Martinez, “The Use of Habituation in the Study of the Effects of Infantile Malnutrition,” Developmental Psychobiology, Vol. 8, No. 6, 1975, pp. 541-546. doi:10.1002/dev.420080611
[33] D. A. Wilson and M. Leon, “Abrupt Decrease in Synaptic Inhibition in the Postnatal Rat Olfactory Bulb,” Developmental Brain Research, Vol. 430, No. 1, 1987, pp. 134-138. doi:10.1016/0165-3806(87)90183-0
[34] N. Mandairon, C. Stack, C. Kiselycznyk and C. Linster, “Broad Activation of the Olfactory Bulb Produces Long-Lasting Changes in Odor Perception,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 103, No. 36, 2006, pp. 13543-13548. doi:10.1073/pnas.0602750103
[35] A. M. McNamara, P. D. Magidson, C. Linster, D. A. Wilson and T. A. Cleland, “Distinct Neural Mechanisms Mediate Olfactory Memory Formation at Different Time Scales,” Learning & Memory, Vol. 15, No. 3, 2012, pp. 117-125. doi:10.1101/lm.785608
[36] M. R. Rosenzweigh and E. L. Bennett, “Psychobiology of Plasticity: Effects of Training and Experience on Brain and Behavior,” Behavioral Brain Research, Vol. 78, No. 1, 1996, pp. 57-65. doi:10.1016/0166-4328(95)00216-2
[37] J. H. McLean, A. Darby-King and W. S. Bonnell, “Neonatal Olfactory Sensory Deprivation Decreases BDNF in the Olfactory Bulb of the Rat,” Developmental Brain Research, Vol. 128, No. 1, 2001, pp. 17-24. doi:10.1016/S0165-3806(01)00144-4
[38] F. Cirulli, L. T. Bonsignore, A. Venerosi, A. Valanzano, F. Chiarotti and E. Alleva, “Long-Term Effects of Acute Perinatal Asphyxia on Rat Maternal Behavior,” Neurotoxicology and Teratology, Vol. 25, No. 5, 2003, pp. 571-578. doi:10.1016/S0892-0362(03)00035-7
[39] C. A. Turner, M. H. Lewis and M. A. King, “Environmental Enrichment: Effects on Stereotyped Behavior and Dendritic Morphology,” Developmental Psychobiology, Vol. 43, No. 1, 2003, pp. 20-27. doi:10.1002/dev.10116
[40] R. M. Sullivan, D. A. Wilson, C. Lemon and G. A. Gerhardt, “Bilateral 6-OHDA Lesions of the Locus Coeruleus Impair Associative Olfactory Learning in Newborn Rats,” Brain Research, Vol. 643, No. 1-2, 1994, pp. 306-309. doi:10.1016/0006-8993(94)90038-8
[41] A. S. Fleming, D. H. O’Day and G. W. Kraemer, “Neurobiology of Mother-Infant Interactions: Experience and Central Nervous System Plasticity across Development and Generations,” Neuroscience Biobehavioral Reviews, Vol. 23, No. 5, 1999, pp. 673-685. doi:10.1016/S0149-7634(99)00011-1
[42] A. C. Tang, “Neonatal Exposure to Novel Environment Enhances Hippocampal-Dependent Memory Function during Infancy and Adulthood,” Learning and Memory, Vol. 8, No. 5, 2001, pp. 257-264. doi:10.110/1m.43101
[43] S. Macrì and H. Würbel, “Developmental Plasticity of HPA and Fear Responses in Rats: A Critical Review of the Maternal Mediation Hypothesis,” Hormones and Behavior, Vol. 50, No. 5, 2006, pp. 667-680. doi:10.1016/j.yhbeh.2006.06.015
[44] E. M. Ables, L. M. Kay and J. M. Mateo, “Rats Assess Degree of Relatedness from Human Odors,” Physiology and Behavior, Vol. 90, No. 5, 2007, pp. 726-732. doi:10.1016/j.physbeh.2006.12.012
[45] M Shimozuru, T. Kikusui, Y. Takeuchi and Y. Mori, “Discrimination of Individuals by Odor in Mongolian Gerbils, Meiornes unguiculates,” Zoological Science, Vol. 24, No. 5, 2007, pp. 427-433. doi:10.2108/zsj.24.427
[46] C. R. Almli, M. A. Henault, C. A. Velozo and J. P. Morgane, “Ontogeny of Electrical Activity of Main Olfactory Bulb in Freely-Moving Normal and Malnourished Rats,” Developmental Brain Research, Vol. 18, No. 1-2, 1985, pp. 1-11. doi:10.1016/0165-3806(85)90245-7
[47] N. E. Cordoba M. P. Arolfo, J. D. Brioni and O. A. Orsingher, “Perinatal Undernutrition Impairs Spatial Learning in Recovered Adult Rats,” Acta Physiologica Pharmacologica Therapeutic Latinoamerica, Vol. 44, No. 3, 1994, pp. 70-76.

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