Share This Article:

Intrauterine Exposure to Chronic 22 kHz Sound Affects Inhibitory Avoidance and Serotonergic Parameters in Forebrain Areas of Dams and Rat Offspring

Abstract Full-Text HTML XML Download Download as PDF (Size:1168KB) PP. 25-39
DOI: 10.4236/jbbs.2015.52003    3,511 Downloads   3,985 Views   Citations

ABSTRACT

In the present study we evaluated the effects of chronic exposure to sounds at 22 kHz during pregnancy on the central serotonergic and behavioral parameters in Wistar rat dams after the suckling period and on their male rat offspring. In addition, we also assessed the effects of an acute 22 kHz sound, associated with the chronic intrauterine exposure, on the emotional responses of adult offspring. The primary hypothesis was that experiencing 22 kHz stimuli during an early stage of development would interfere with brain serotonergic parameters and, later, with the adult rat’s defensive responses. The corollary question was whether a 22 kHz sound exposure would differentially affect inhibitory avoidance and escape responses and central serotonergic parameters. Female rats were divided into four groups: non-pregnant control; non-pregnant chronic exposure; pregnant control; and pregnant chronic exposure. Male offspring were divided into four groups: chronic intrauterine sound exposure; acute sound exposure in adulthood; chronic intrauterine exposure with acute exposure in adulthood; and no exposure. Chronic sound exposure affected inhibitory avoidance and serotonergic parameters in female rats. For offspring, there was an interaction between chronic and acute sound exposure effects on inhibitory avoidance response but not on escape response. There were significant effects of chronic intrauterine exposure on serotonin turnover in the hippocampus and PFC of females. For offspring, the turnover was increased by chronic exposure only in PFC, and in amygdala it was increased by acute exposure. These results illuminate the potential of an early acoustic sound exposure for causing central serotonergic and emotional behavioral changes that can persist into later periods of life.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

da Silva Oliveira, P. , Daniel, A. , Nunes, P. , Costa, K. , Yehia, H. and Ribeiro, A. (2015) Intrauterine Exposure to Chronic 22 kHz Sound Affects Inhibitory Avoidance and Serotonergic Parameters in Forebrain Areas of Dams and Rat Offspring. Journal of Behavioral and Brain Science, 5, 25-39. doi: 10.4236/jbbs.2015.52003.

References

[1] Anderson, J.W. (1954) The Production of Ultrasonic Sounds by Laboratory Rats and Other Mammals. Science, 119, 808-809.
http://dx.doi.org/10.1126/science.119.3101.808
[2] Brudzynski, S.M., et al. (1993) Analysis of 22 kHz Ultrasonic Vocalization in Laboratory Rats: Long and Short Calls. Physiology & Behavior, 54, 215-221.
http://dx.doi.org/10.1016/0031-9384(93)90102-L
[3] Wohr, M., Borta, A. and Schwarting, R.K. (2005) Overt Behavior and Ultrasonic Vocalization in a Fear Conditioning Paradigm: A Dose-Response Study in the Rat. Neurobiology of Learning and Memory, 84, 228-240.
http://dx.doi.org/10.1016/j.nlm.2005.07.004
[4] Wohr, M. and Schwarting, R.K. (2013) Affective Communication in Rodents: Ultrasonic Vocalizations as a Tool for Research on Emotion and Motivation. Cell and Tissue Research, 354, 81-97.
http://dx.doi.org/10.1007/s00441-013-1607-9
[5] Blanchard, R.J., et al. (1992) Sex Differences in the Incidence and Sonographic Characteristics of Antipredator Ultrasonic Cries in the Laboratory Rat (Rattusnorvegicus). Journal of Comparative Psychology, 106, 270-277.
http://dx.doi.org/10.1037/0735-7036.106.3.270
[6] Thomas, D.A., Takahashi, L.K. and Barfield, R.J. (1983) Analysis of Ultrasonic Vocalizations Emitted by Intruders during Aggressive Encounters among Rats (Rattusnorvegicus). Journal of Comparative Psychology, 97, 201-206.
http://dx.doi.org/10.1037/0735-7036.97.3.201
[7] Parsana, A.J., Li, N. and Brown, T.H. (2012) Positive and Negative Ultrasonic Social Signals Elicit Opposing Firing Patterns in Rat Amygdala. Behavioural Brain Research, 226, 77-86.
http://dx.doi.org/10.1016/j.bbr.2011.08.040
[8] Sadananda, M., Wohr, M. and Schwarting, R.K. (2008) Playback of 22-kHz and 50-kHz Ultrasonic Vocalizations Induces Differential c-fos Expression in Rat Brain. Neuroscience Letters, 435, 17-23.
http://dx.doi.org/10.1016/j.neulet.2008.02.002
[9] Jelen, P., Soltysik, S. and Zagrodzka, J. (2003) 22-kHz Ultrasonic Vocalization in Rats as an Index of Anxiety but Not Fear: Behavioral and Pharmacological Modulation of Affective State. Behavioural Brain Research, 141, 63-72.
http://dx.doi.org/10.1016/S0166-4328(02)00321-2
[10] Lucas, A. (1994) Role of Nutritional Programming in Determining Adult Morbidity. Archives of Disease in Childhood, 71, 288-290.
http://dx.doi.org/10.1136/adc.71.4.288
[11] Whimbey, A.E. and Denenberg, V.H. (1967) Experimental Programming of Life Histories: The Factor Structure Underlying Experimentally Created Individual Differences. Behaviour, 29, 296-314.
http://dx.doi.org/10.1163/156853967X00163
[12] Lucas, A. (1991) Programming by Early Nutrition in Man. Ciba Foundation Symposium, 156, 38-50 (Discussion 50-55).
[13] Lesage, J., Del-Favero, F., Leonhardt, M., Louvart, H., Maccari, S., Vieau, D. and Darnaudery, M. (2004) Prenatal Stress Induces Intrauterine Growth Restriction and Programmes Glucose Intolerance and Feeding Behaviour Disturbances in the Aged Rat. Journal of Endocrinology, 181, 291-296.
http://dx.doi.org/10.1677/joe.0.1810291
[14] Matsumoto, M., Yoshioka, M. and Togashi, H. (2009) Early Postnatal Stress and Neural Circuit Underlying Emotional Regulation. International Review of Neurobiology, 85, 95-107.
http://dx.doi.org/10.1016/S0074-7742(09)85007-1
[15] Anacker, C., O’Donnell, K.J. and Meaney, M.J. (2014) Early Life Adversity and the Epigenetic Programming of Hypothalamic-Pituitary-Adrenal Function. Dialogues in Clinical Neuroscience, 16, 321-333.
[16] Levine, S. (2002) Regulation of the Hypothalamic-Pituitary-Adrenal Axis in the Neonatal Rat: The Role of Maternal Behavior. Neurotoxicity Research, 4, 557-564.
http://dx.doi.org/10.1080/10298420290030569
[17] Vazquez, D.M., Bailey, C., Dent, G.W., Okimoto, D.K., Steffek, A., López, J.F. and Levine, S. (2006) Brain Corticotropin-Releasing Hormone (CRH) Circuits in the Developing Rat: Effect of Maternal Deprivation. Brain Research, 1121, 83-94.
http://dx.doi.org/10.1016/j.brainres.2006.08.104
[18] Kim, C.H., Lee, S.-C., Shin, J.W., Chung, K.-J., Lee, S.-H., Shin, M.-S., et al. (2013) Exposure to Music and Noise during Pregnancy Influences Neurogenesis and Thickness in Motor and Somatosensory Cortex of Rat Pups. International Neurourology Journal, 17, 107-113.
http://dx.doi.org/10.5213/inj.2013.17.3.107
[19] Graeff, F.G., Viana, M.B. and Tomaz, C. (1993) The Elevated T Maze, a New Experimental Model of Anxiety and Memory: Effect of Diazepam. Brazilian Journal of Medical and Biological Research, 26, 67-70.
[20] Pellow, S., Chopin, P., File, S.E. and Briley, M. (1985) Validation of Open: Closed Arm Entries in an Elevated Plus-Maze as a Measure of Anxiety in the Rat. Journal of Neuroscience Methods, 14, 149-167.
http://dx.doi.org/10.1016/0165-0270(85)90031-7
[21] Graeff, F.G., Netto, C.F. and Zangrossi Jr., H. (1998) The Elevated T-Maze as an Experimental Model of Anxiety. Neuroscience & Biobehavioral Reviews, 23, 237-246.
http://dx.doi.org/10.1016/S0149-7634(98)00024-4
[22] Viana, M.B., Tomaz, C. and Graeff, F.G. (1994) The Elevated T-Maze: A New Animal Model of Anxiety and Memory. Pharmacology Biochemistry and Behavior, 49, 549-554.
http://dx.doi.org/10.1016/0091-3057(94)90067-1
[23] Zangrossi Jr., H. and Graeff, F.G. (1997) Behavioral Validation of the Elevated T-Maze: A New Animal Model of Anxiety. Brain Research Bulletin, 44, 1-5.
http://dx.doi.org/10.1016/S0361-9230(96)00381-4
[24] Graeff, F.G. (2007) Anxiety, Panic and the Hypothalamic-Pituitary-Adrenal Axis. The Revista Brasileira de Psiquiatria, 29, S3-S6.
http://dx.doi.org/10.1590/S1516-44462007000500002
[25] Graeff, F.G., Viana, M.B. and Mora, P.O. (1996) Opposed Regulation by Dorsal Raphe Nucleus 5-HT Pathways of Two Types of Fear in the Elevated T-Maze. Pharmacology Biochemistry and Behavior, 53, 171-177.
http://dx.doi.org/10.1016/0091-3057(95)02012-8
[26] Zangrossi Jr., H. and Graeff, F.G. (2014) Serotonin in Anxiety and Panic: Contributions of the Elevated T-Maze. Neuroscience Biobehavioral Reviews, 46, 397-406.
[27] Escribano, B., Quero, I., Feijóo, M., Tasset, I., Montilla, P. and Túnez, I. (2013) Role of Noise and Music as Anxiety Modulators: Relationship with Ovarian Hormones in the Rat. Applied Animal Behaviour Science, 152, 73-82.
[28] de Freitas-Silva, D.M., de Souza Resende, L., Pereira, S.R.C., Franco, G.C. and Ribeiro, A.M. (2010) Maternal Thiamine Restriction during Lactation Induces Cognitive Impairments and Changes in Glutamate and GABA Concentrations in Brain of Rat Offspring. Behavioural Brain Research, 211, 33-40.
http://dx.doi.org/10.1016/j.bbr.2010.03.002
[29] Goldman, J.M., Murr, A.S. and Cooper, R.L. (2007) The Rodent Estrous Cycle: Characterization of Vaginal Cytology and Its Utility in Toxicological Studies. Birth Defects Research Part B: Developmental and Reproductive Toxicology, 80, 84-97.
http://dx.doi.org/10.1002/bdrb.20106
[30] Furtak, S.C., Allen, T.A. and Brown, T.H. (2007) Single-Unit Firing in Rat Perirhinal Cortex Caused by Fear Conditioning to Arbitrary and Ecological Stimuli. Journal of Neuroscience, 27, 12277-12291.
http://dx.doi.org/10.1523/JNEUROSCI.1653-07.2007
[31] Paxinos, G., et al. (1985) Bregma, Lambda and the Interaural Midpoint in Stereotaxic Surgery with Rats of Different Sex, Strain and Weight. Journal of Neuroscience Methods, 13, 139-143.
http://dx.doi.org/10.1016/0165-0270(85)90026-3
[32] Paul, E.D. and Lowry, C.A. (2013) Functional Topography of Serotonergic Systems Supports the Deakin/Graeff Hypothesis of Anxiety and Affective Disorders. Journal of Psychopharmacology, 27, 1090-1106.
http://dx.doi.org/10.1177/0269881113490328
[33] Oliveira-Silva, I.F., Pintoa, L., Pereirab, S.R.C., Ferrazc, V.P., Barbosad, A.J.A., Coelho, V.A.A., et al. (2007) Age-Related Deficit in Behavioural Extinction Is Counteracted by Long-Term Ethanol Consumption: Correlation between 5-HIAA/5HT Ratio in Dorsal Raphe Nucleus and Cognitive Parameters. Behavioural Brain Research, 180, 226-234.
http://dx.doi.org/10.1016/j.bbr.2007.03.012
[34] Shannon, N.J., Gunnet, J.W. and Moore, K.E. (1986) A Comparison of Biochemical Indices of 5-Hydroxytryptaminergic Neuronal Activity Following Electrical Stimulation of the Dorsal Raphe Nucleus. Journal of Neurochemistry, 47, 958-965.
http://dx.doi.org/10.1111/j.1471-4159.1986.tb00704.x
[35] Beckett, S.R.G., Aspley, S., Graham, M. and Marsden, C.A. (1996) Pharmacological Manipulation of Ultrasound Induced Defense Behaviour in the Rat. Psychopharmacology, 127, 384-390.
http://dx.doi.org/10.1007/s002130050102
[36] Escribano, B., Quero, I., Feijóo, M., Tasset, I., Montilla, P. and Túnez, I. (2014) Role of Noise and Music as Anxiety Modulators: Relationship with Ovarian Hormones in the Rat. Applied Animal Behaviour Science, 152, 73-82.
[37] Nishio, H., Kasuga, S., Ushijima, M. and Harada, Y. (2001) Prenatal Stress and Postnatal Development of Neonatal Rats—Sex-Dependent Effects on Emotional Behavior and Learning Ability of Neonatal Rats. International Journal of Developmental Neuroscience, 19, 37-45.
http://dx.doi.org/10.1016/S0736-5748(00)00070-8
[38] Naqvi, F., Haider, S., Perveen, T. and Haleem, D.J. (2012) Sub-Chronic Exposure to Noise Affects Locomotor Activity and Produces Anxiogenic and Depressive like Behavior in Rats. Pharmacological Reports, 64, 64-69.
http://dx.doi.org/10.1016/S1734-1140(12)70731-4
[39] Uran, S.L., Caceres, L.G. and Guelman, L.R. (2010) Effects of Loud Noise on Hippocampal and Cerebellar-Related Behaviors. Brain Research, 1361, 102-114. http://dx.doi.org/10.1016/j.brainres.2010.09.022
[40] Morozova, A.Y., Zubkov, E.A., Storozheva, Z.I., Kekelidze, Z.I. and Chekhonin, V.P. (2013) Effect of Ultrasonic Irradiation on the Development of Symptoms of Depression and Anxiety in Rats. Bulletin of Experimental Biology and Medicine, 154, 740-743.
http://dx.doi.org/10.1007/s10517-013-2044-1
[41] Grissom, N. and Bhatnagar, S. (2009) Habituation to Repeated Stress: Get Used to It. Neurobiology of Learning and Memory, 92, 215-224.
http://dx.doi.org/10.1016/j.nlm.2008.07.001
[42] Masini, C.V., Babb, J.A., Nyhuis, T.J., Day, H.E.W. and Campeau, S. (2012) Auditory Cortex Lesions Do Not Disrupt Habituation of HPA Axis Responses to Repeated Noise Stress. Brain Research, 1443, 18-26.
http://dx.doi.org/10.1016/j.brainres.2012.01.002
[43] Wallenius, M.A. (2004) The Interaction of Noise Stress and Personal Project Stress on Subjective Health. Journal of Environmental Psychology, 24, 167-177.
http://dx.doi.org/10.1016/j.jenvp.2003.12.002
[44] Abrams, R., Gerhardt, K. and Antonelli, P. (1998) Fetal Hearing. Developmental Psychobiology, 33, 1-3.
http://dx.doi.org/10.1002/(SICI)1098-2302(199807)33:1<1::AID-DEV1>3.0.CO;2-P
[45] Antonelli, P.J., Gerhardt, K., Abrams, R. and Huang, X. (2002) Fetal Central Auditory System Metabolic Response to Cochlear Implant Stimulation. Otolaryngology—Head and Neck Surgery, 127, 131-137.
http://dx.doi.org/10.1067/mhn.2002.126899
[46] Hepper, P.G. and Shahidullah, B.S. (1994) Development of Fetal Hearing. Archives of Disease in Childhood, 71, F81-F87.
http://dx.doi.org/10.1136/fn.71.2.F81
[47] Geal-Dor, M., Freeman, S., Li, G. and Sohmer, H. (1993) Development of Hearing in Neonatal Rats: Air and Bone Conducted ABR Thresholds. Hearing Research, 69, 236-242.
http://dx.doi.org/10.1016/0378-5955(93)90113-F
[48] Saliu, A. (2011) The Development of Hearing in Rats: Reliability of Wave 1 as a Determinant of Auditory Maturation and Contributions of Peripheral Structure Progression. City College of New York, New York, 33.
[49] Barnett, S.B., Rott, H.-D., ter Haar, G.R., Ziskin, M.C. and Maeda, K. (1997) The Sensitivity of Biological Tissue to Ultrasound. Ultrasound in Medicine & Biology, 23, 805-812.
http://dx.doi.org/10.1016/S0301-5629(97)00027-6
[50] Weinstock, M. (1997) Does Prenatal Stress Impair Coping and Regulation of Hypothalamic-Pituitary-Adrenal Axis? Neuroscience & Biobehavioral Reviews, 21, 1-10.
http://dx.doi.org/10.1016/S0149-7634(96)00014-0
[51] Weinstock, M. (2008) The Long-Term Behavioural Consequences of Prenatal Stress. Neuroscience & Biobehavioral Reviews, 32, 1073-1086.
http://dx.doi.org/10.1016/j.neubiorev.2008.03.002
[52] Hu, L., Yang, J., Song, T.S., Hou, N., Liu, Y., Zhao, X.G., et al. (2014) A New Stress Model, a Scream Sound, Alters Learning and Monoamine Levels in Rat Brain. Physiology & Behavior, 123, 105-113.
http://dx.doi.org/10.1016/j.physbeh.2013.09.010
[53] Lanfumey, L., Mongeau, R., Cohen-Salmon, C. and Hamon, M. (2008) Corticosteroid-Serotonin Interactions in the Neurobiological Mechanisms of Stress-Related Disorders. Neuroscience & Biobehavioral Reviews, 32, 1174-1184.
http://dx.doi.org/10.1016/j.neubiorev.2008.04.006
[54] Graeff, F.G., Garcia-Leal, C., Del-Ben, C.M. and Guimaraes, F.S. (2005) Does the Panic Attack Activate the Hypothalamic-Pituitary-Adrenal Axis? Anais da Academia Brasileira de Ciências, 77, 477-491.
http://dx.doi.org/10.1590/S0001-37652005000300009
[55] Graeff, F.G. (2011) Defense-Related Emotions in Humans. Psychology and Neuroscience, 4, 183-189.
http://dx.doi.org/10.3922/j.psns.2011.2.003
[56] Graeff, F.G. and Zangrossi Jr., H. (2010) The Dual Role of Serotonin in Defense and the Mode of Action of Antidepressants on Generalized Anxiety and Panic Disorders. Central Nervous System Agents in Medicinal Chemistry, 10, 207-217.
http://dx.doi.org/10.2174/1871524911006030207
[57] Graeff, F.G. (2003) Serotonin, Periaqueductal Gray Matter and Panic Disorder. Revista Brasileira de Psiquiatria, 25, 42-45.
http://dx.doi.org/10.1590/S1516-44462003000600010
[58] Sanchez, C., Gruca, P. and Papp, M. (2003) R-Citalopram Counteracts the Antidepressant-Like Effect of Escitalopram in a Rat Chronic Mild Stress Model. Behavioural Pharmacology, 14, 465-470.
[59] Curran, K.P. and Chalasani, S.H. (2012) Serotonin Circuits and Anxiety: What Can Invertebrates Teach Us? Invertebrate Neuroscience, 12, 81-92.
[60] Maron, E., Nutt, D. and Shlik, J. (2012) Neuroimaging of Serotonin System in Anxiety Disorders. Current Pharmaceutical Design, 18, 5699-5708.
http://dx.doi.org/10.2174/138161212803530844
[61] Graeff, F.G. (2002) On Serotonin and Experimental Anxiety. Psychopharmacology, 163, 467-476.
http://dx.doi.org/10.1007/s00213-002-1112-4
[62] Rex, A., Voigt, J.P. and Fink, H. (2005) Anxiety but Not Arousal Increases 5-Hydroxytryptamine Release in the Rat Ventral Hippocampus in Vivo. European Journal of Neuroscience, 22, 1185-1189.
http://dx.doi.org/10.1111/j.1460-9568.2005.04251.x
[63] Midzyanovskaya, I.S., Kuznetsova, G.D., van Luijtelaar, E.L.J.M., van Rijn, C.M., Tuomisto, L. and MacDonald, E. (2006) The Brain 5HTergic Response to an Acute Sound Stress in Rats with Generalized (Absence and Audiogenic) Epilepsy. Brain Research Bulletin, 69, 631-638.
http://dx.doi.org/10.1016/j.brainresbull.2006.03.008
[64] Compan, V. (2007) Do Limits of Neuronal Plasticity Represent an Opportunity for Mental Diseases, Such as Addiction to Food and Illegal Drugs? Use and Utilities of Serotonin Receptor Knock-Out Mice. In: Chattopadhyay, A., Ed., Serotonin Receptors in Neurobiology, CRC Press, Boca Raton.
[65] LeDoux, J. (2007) The Amygdala. Current Biology, 17, R868-R874.
http://dx.doi.org/10.1016/j.cub.2007.08.005
[66] Berretta, S. (2005) Cortico-Amygdala Circuits: Role in the Conditioned Stress Response. Stress, 8, 221-232.
http://dx.doi.org/10.1080/10253890500489395
[67] Shin, L.M. and Liberzon, I. (2010) The Neurocircuitry of Fear, Stress, and Anxiety Disorders. Neuropsychopharmacology, 35, 169-191.
http://dx.doi.org/10.1038/npp.2009.83
[68] van Marle, H.J.F., Hermans, E.J., Qin, S.Z. and Fernández, G. (2009) From Specificity to Sensitivity: How Acute Stress Affects Amygdala Processing of Biologically Salient Stimuli. Biological Psychiatry, 66, 649-655.
http://dx.doi.org/10.1016/j.biopsych.2009.05.014
[69] Leuner, B. and Shors, T.J. (2012) Stress, Anxiety, and Dendritic Spines: What Are the Connections? Neuroscience, 251, 108-119.
http://dx.doi.org/10.1016/j.neuroscience.2012.04.021
[70] Mahan, A.L. and Ressler, K.J. (2012) Fear Conditioning, Synaptic Plasticity and the Amygdala: Implications for Posttraumatic Stress Disorder. Trends in Neurosciences, 35, 24-35.
http://dx.doi.org/10.1016/j.tins.2011.06.007
[71] McEwen, B.S., Eiland, L., Hunter, R.G. and Miller, M.M. (2012) Stress and Anxiety: Structural Plasticity and Epigenetic Regulation as a Consequence of Stress. Neuropharmacology, 62, 3-12.
http://dx.doi.org/10.1016/j.neuropharm.2011.07.014
[72] Mitra, R., Jadhav, S., McEwen, B.S., Vyas, A. and Chattarji, S. (2005) Stress Duration Modulates the Spatiotemporal Patterns of Spine Formation in the Basolateral Amygdala. Proceedings of the National Academy of Sciences of the United States of America, 102, 9371-9376.
http://dx.doi.org/10.1073/pnas.0504011102
[73] Mitra, R., Ferguson, D. and Sapolsky, R.M. (2009) SK2 Potassium Channel Overexpression in Basolateral Amygdala Reduces Anxiety, Stress-Induced Corticosterone Secretion and Dendritic Arborization. Molecular Psychiatry, 14, 847-855.
[74] Roozendaal, B., McReynolds, J.R., Van der Zee, E.A., Lee, S., McGaugh, J.L. and McIntyre, C.K. (2009) Glucocorticoid Effects on Memory Consolidation Depend on Functional Interactions between the Medial Prefrontal Cortex and Basolateral Amygdala. Journal of Neuroscience, 29, 14299-14308.
http://dx.doi.org/10.1523/JNEUROSCI.3626-09.2009
[75] Vyas, A., Jadhav, S. and Chattarji, S. (2006) Prolonged Behavioral Stress Enhances Synaptic Connectivity in the Basolateral Amygdala. Neuroscience, 143, 387-393.
http://dx.doi.org/10.1016/j.neuroscience.2006.08.003

  
comments powered by Disqus

Copyright © 2019 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.