Effects of Pre- and Neonatal Undernutrition on Long-Term Hearing Cognition of the Rat — Oak Academic Publishing
ReviewOpen AccessGoogle Scholar indexed
Effects of Pre- and Neonatal Undernutrition on Long-Term Hearing Cognition of the Rat
Institute of Neurobiology, Department of Developmental Neurobiology and Neurophysiology, Universidad Nacional Autónoma de México, Campus UNAM Juriquilla, Querétaro, México
,
Institute of Neurobiology, Department of Developmental Neurobiology and Neurophysiology, Universidad Nacional Autónoma de México, Campus UNAM Juriquilla, Querétaro, México
,
Institute of Neurobiology, Department of Developmental Neurobiology and Neurophysiology, Universidad Nacional Autónoma de México, Campus UNAM Juriquilla, Querétaro, México
1 Institute of Neurobiology, Department of Developmental Neurobiology and Neurophysiology, Universidad Nacional Autónoma de México, Campus UNAM Juriquilla, Querétaro, México
2 Institute of Neurobiology, Department of Developmental Neurobiology and Neurophysiology, Universidad Nacional Autónoma de México, Campus UNAM Juriquilla, Querétaro, México
3 Institute of Neurobiology, Department of Developmental Neurobiology and Neurophysiology, Universidad Nacional Autónoma de México, Campus UNAM Juriquilla, Querétaro, México
Experimental evidence in the rat suggests that perinatal undernutrition, associated with sensory and hormonal deficiencies, interferes with brain network integrative actions. We review peripheral and central morpho-functional alterations related to early food restriction along with the auditory relays, and their connections with the limbic system, which are essential for motivation-emotional arousal. The findings indicated that different morpho-functional alterations in the auditory system permanently affect the brainstem, the reticular thalamic nucleus, and the prefrontal and auditory cortices. Moreover, data showed the noxious role of early food restriction and the external ear occlusion on the distal portions of dendritic arbor measurements, in the cochlea, nucleus ambiguous and motor cortical pyramids. These anatomical alterations also correlated with deficiencies in the dynamic motor and auditory cognitive brain plasticity. Food restriction-related deficiencies in the motor-emotional-behavioral arousal systems may be useful to understand long-term cognitive disorders in humans.
D’Amato, F.R.D., Scalera, E., Sarli, C. and Moles A. (2005) Pup Call, Mothers Rush: Does Maternal Responsiveness Affect the Amount of Ultrasonic Vocalizations in Mouse Pups? Behavior Genetics, 35, 103-112. https://doi.org/10.1007/s10519-004-0860-9
Harmon, K.M., Cromwell, H.C., Burgdorf, J.R., Moskal, S.M., Brudzynski, R.A., Kroes, R.A. and Panksepp, J. (2008) Rats Selectively Bred for Low Levels of 50 KHz Ultrasonic Vocalizations Exhibit Alterations in Early Social Motivation. Developmental Psychobiology, 50, 322-331. https://doi.org/10.1002/dev.20294
MacLean, P. (1990) The Triune Brain in Evolution: Role in Paleocerebral Functions. Plenum Press, New York.
Panksepp, J. (1998) Affective Neuroscience: The Foundations of Human and Animal Emotions. Oxford University Press, New York.
Hébert, R., Langlois, J.M. and Dussault, J.H. (1985) Permanent Defects in Rat Peripheral Auditory Function Following Perinatal Hypothyroidism: Determination of a Critical Period. Developmental Brain Research, 23, 161-170. https://doi.org/10.1016/0165-3806(85)90037-9
Torrero, C., Regalado, M., Perez, E., Loranca, A. and Salas, M. (1999) Effects of Neonatal Undernutrition and Binaural Ear Occlusion on Neuronal Development of the Superior Olivary Complex of Rats. Biology of the Neonate, 75, 259-271. https://doi.org/10.1159/000014103
Tonkiss, J., Bonnie, K.E., Hudson, J.I., Shultz, P.I., Duran, P. and Galler, J.R. (2003) Ultrasonic Call Characteristics of Rat Pups Are Altered Following Prenatal Malnutrition. Developmental Psychobiology, 43, 90-101. https://doi.org/10.1002/dev.10124
Chen, S., Liang, T., Zhou, F.H., Cao, Y., Wang, Ch., Wang, F.Y., Li, F., Zhou, X.F., Zhang, J.Y. and Li, Ch.Q. (2019) Regular Music Exposure in Juvenile Rats Facilitates Conditioned Fear Extinction and Reduces Anxiety after Food Shock in Adulthood. Biomedical Research International, 2019, Article ID: 8740674. https://doi.org/10.1155/2019/8740674
Salas, M., Ortiz-Valladares, M., Regalado, M. and Torrero, C. (2020) Neuronal c-Fos Reactivity of Medial Prefrontal Cortex and Basolateral Amygdala in Perinatally Underfed Lactating Wistar Rats. Journal of Behavioral and Brain Sciences, 10, 548-561. https://doi.org/10.4236/jbbs.2020.1012034
Knipper, M., Zinn, C., Maier, H., Praetorious, M., Rohbock, K., Köpschall, I. and Zimmermann, U. (2000) Thyroid Hormone Deficiency Before the Onset of Hearing Causes Irreversible Damage to Peripheral and Central Auditory Systems. Journal of Neurophysiology, 83, 3101-3112. https://doi.org/10.1152/jn.2000.83.5.3101
Salcedo, C., Torrero, C., Regalado, M., Rubio, L. and Salas, M. (2018) Effects of Pre- and Neonatal Undernutrition on the Kyphotic Response and c-Fos Activity in the Caudal Periaqueductal Gray of Primiparous Lactating Wistar Rats. Physiology and Behavior, 185, 87-94. https://doi.org/10.1016/j.physbeh.2017.12.020
Salas, M., Díaz, S. and Nieto, A. (1974) Effect of Neonatal Food Deprivation on Cortical Spines and Dendritic Development of the Rat. Brain Research, 73, 139-144. https://doi.org/10.1016/0006-8993(74)91012-9
Math, F. and Davrainville, J.L. (1980) Electrophysiological Study of the Postnatal Development of Mitral Cell Activity in the Rat Olfactory Bulb. Influence of Undernutrition. Brain Research, 194, 223-227. https://doi.org/10.1016/0006-8993(80)91333-5
Salas, M. (1980) Effects of Early Undernutrition on Dendritic Spines of Cortical Pyramidal Cells in the Rat. Developmental Neuroscience, 3, 109-117. https://doi.org/10.1159/000112384
Quirk, G.J., Mejia W.R., Hesse, H. and Su, H. (1995) Early Malnutrition Followed by Nutritional Restoration Lowers the Conduction Velocity and Excitability of the Corticospinal Tract. Brain Research, 670, 277-282. https://doi.org/10.1016/0006-8993(94)01285-P
Salas, M., Torrero, C., Regalado, M. and Rubio, L. (2015) Effects of Perinatal Undernutrition on the Basilar Dendritic Arbor of the Anterior Cingulate Pyramidal Neurons in Lactating Dams. Acta Neurobiologiae Experimentalisl, 75, 372-380.
Ortiz-Valladares, M., Torrero, C., Regalado, M. and Salas, M. (2018) Late-Emerging Effects of Perinatal Undernutrition in Neuronal Limbic Structures Underlying the Maternal Response in the Rat. Brain Research, 1700, 31-40. https://doi.org/10.1016/j.brainres.2018.06.033
Eayrs, J.T. and Horn, G. (1955) The Development of the Cerebellar Cortex in Hypothyroid and Starved Rats. Anatomical Records, 12, 53-61. https://doi.org/10.1002/ar.1091210105
Clos, J. and Legrand, J. (1970) Influence de la déficience thyroïdienne et de la sous-alimentation sur la croissance et la myélinisation des fibres nerveuses du nerf sciatique chez le jeune rat blanc.étude au microscopeélectronique: Effects of Thyroid Deficiency and Underfeeding on Growth and Myelination of the Sciatic Nerve Fibers in the Young Rat. An Electron Microscopic Study. Brain Research, 22, 285-297. https://doi.org/10.1016/0006-8993(70)90472-5
Lewis, P.D., Balázs, R, Patel, A.J. and Johnson, A.L. (1975) The Effect of Undernutrition in Early Life on Cell Generation in the Rat Brain. Brain Research, 83, 235-247. https://doi.org/10.1016/0006-8993(75)90933-6
Morgan, B.L.G. and Naismith, D.J. (1982) The Effect of Early Postnatal Undernutrition on the Growth and Development of the Rat Brain. Journal of Nutrition, 48, 15-23. https://doi.org/10.1079/BJN19820083
Schanberg, S.M., Evoniuk, G. and Kuhn, C.M. (1984) Tactile and Nutritional Aspects of Maternal Care: Specific Regulators of Neuroendocrine Function and Cellular Development. Proceedings of the Society for Experimental Biology and Medicine, 175, 135-146. https://doi.org/10.3181/00379727-175-41779
Ruiz-Marcos, A., Cartagena-Abella, P., Martinez-Galan, J.R., Calvo, R., Morreale De Escobar, G. and Escobar Del Rey, F. (1994) Thyroxine Treatment and Recovery of Pyramidal Cells of the Cerebral Cortex from Changes Induced by Juvenile-Onset Hypothyroidism. Journal of Neurobiology, 25, 808-818. https://doi.org/10.1002/neu.480250706
Felix, J., Regalado, M., Torrero, C. and Salas, M. (2014) Retrieval of Pups by Female Rats Undernourished during the Pre- and Neonatal Period. Journal of Behavioral Brain Science, 4, 325-333. https://doi.org/10.4236/jbbs.2014.47033
Watanabe, Y., Gould, E. and McEwen, B.S. (1992) Stress Induces Atrophy of Apical Dendrites of Hippocampal CA3 Pyramidal Neurons. Brain Research, 588, 341-345. https://doi.org/10.1016/0006-8993(92)91597-8
Salas, M., Torrero, C., Regalado, M. and Perez, E. (2002) Retrieving of Pups by Neonatally Stressed Mothers. Nutritional Neuroscience, 5, 399-405. https://doi.org/10.1080/1028415021000055943
Cook, S.C. and Wellman, C.I. (2004) Chronic Stress Alters Dendritic Morphology in Rat Medial Prefrontal Cortex. Journal of Neurobiology, 60, 236-248. https://doi.org/10.1002/neu.20025
Macri, S. and Würbel, H. (2006) Developmental Plasticity of HPA and Fear Responses in Rats: A Critical Review of the Maternal Mediation Hypothesis. Hormones and Behavior, 50, 667-680. https://doi.org/10.1016/j.yhbeh.2006.06.015
Grace, C.E., Kim, S.J. and Rogers, J.M. (2011) Maternal Influences on Epigenetic Programming of the Developing Hypothalamic-Pituitary-Adrenal Axis. Birth Defects Research Part A: Clinical Molecular Teratology, 91, 797-805. https://doi.org/10.1002/bdra.20824
Callison, D.A. and Spencer, J.W. (1968) Effect of Chronic Undernutrition and/or Visual Deprivation upon the Visual Evoked Potential from the Developing Rat Brain. Developmental Psychobiology, 1, 196-204. https://doi.org/10.1002/dev.420010308
Salas, M. and Cintra, L. (1973) Nutritional Influences upon Somatosensory Evoked Responses during Development in the Rat. Physiology and Behavior, 10, 1019-1022. https://doi.org/10.1016/0031-9384(73)90182-0
Alberts, J.R. and Cramer, C.P. (1988) Ecology and Experience. In: Blass, E.M., Ed., Developmental Psychobiology and Behavioral Ecology, Handbook of Behavioral Neurobiology, Vol. 9, Springer, Boston, 1-39. https://doi.org/10.1007/978-1-4684-5421-5_1
Kelly, J.B., Judge, P.W. and Fraser, I.H. (1987) Development of the Auditory Orientation Response in the Albino Rat (Rattus norvegicus). Journal of Comparative Psychology, 101, 60-66. https://doi.org/10.1037/0735-7036.101.1.60
Soriano, O., Regalado, M., Torrero, C. and Salas, M. (2006) Contributions of Undernutrition and Handling to Huddling Development of Rats. Physiology and Behavior, 89, 543-551. https://doi.org/10.1016/j.physbeh.2006.07.021
Lavado-Autric, R., Ausó, E., Garcia-Velasco, J.V., Arufe, M., Escobar Del Rey, F., Berbel, P. and Morreale De Escobar, G. (2003) Early Maternal Hypothyroxinemia Alters Histogenesis and Cerebral Cortex Cytoarchitecture of the Progeny. Journal Clinical Investigation, 111, 1073-1082. https://doi.org/10.1172/JCI200316262
Salas, M., Torrero, C. and Regalado, M. (2007) Recuperación morfológica y funcional de estructuras cerebrales afectadas por la desnutrición perinatal: Participación de las hormonas tiroideas. Proceedings of 50th Annual Course of the Mexican Physiological Society, Puebla, September 8-9 2007, 52-58.
Porterfield, S.P. and Hendrich, C.E. (1993) The Role of Thyroid Hormones in Prenatal and Neonatal Neurological Development—Current Perspectives. Endocrine Review, 14, 94-106. https://doi.org/10.1210/edrv-14-1-94
álaez, C., Calvo, M.J., Obregon, M.J. and Pascual-Leone, A.M. (1992) Thyroid Hormones and 5’-Deiodinase Activity in Neonatal Undernourished Rats. Endocrinology, 130, 773-779. https://doi.org/10.1210/endo.130.2.1733724
Gabrion, J., Legrand, C., Mercier, B., Harricane, M.C. and Uziel, A. (1984) Microtubules in the Cochlea of the Hypothyroid Developing Rat. Hearing Research, 13, 203-214. https://doi.org/10.1016/0378-5955(84)90074-1
Uziel, A. (1986) Periods of Sensitivity to Thyroid Hormone during the Development of the Organ of Corti. Acta Oto-Laryngologica, 101, 23-27. https://doi.org/10.3109/00016488609122726
Comer, C.P. and Norton, S. (1982) Effects of Perinatal Methimazole Exposure on a Developmental Test Battery for Neurobehavioral Toxicity in Rats. Toxicology and Applied Pharmacology, 63, 133-141. https://doi.org/10.1016/0041-008X(82)90032-1
Goldey, E.S., Kehn, L.S., Rehnberg, G.L. and Crofton, K.M. (1995) Effect of Developmental Hypothyroidism on Auditory and Motor Function in the Rat. Toxicology and Applied Pharmacology, 135, 67-76. https://doi.org/10.1006/taap.1995.1209
Schapiro, S., Salas, M. and Vukovich, K. (1970) Hormonal Effects on Ontogeny of Swimming Ability in the Rat: Assessment of Central Nervous System Development. Science, 168, 147-151. https://doi.org/10.1126/science.168.3927.147
Altman, J., Sudarshan, K., Das, G.D., MacCormick, N. and Barnes, D. (1971) The Influence of Nutrition on Neural and Behavioral Development. III. Development of Some Motor, Particularly Locomotor Patterns during Infancy. Developmental Psychobiology, 4, 97-114. https://doi.org/10.1002/dev.420040202
Salas, M. (1972) Effects of Early Malnutrition on the Development of Swimming Ability in the Rat. Physiology and Behavior, 8, 119-122. https://doi.org/10.1016/0031-9384(72)90137-0
Salas, M., Pulido, S., Torrero, C. and Escobar, C. (1991) Neonatal Undernutrition and Self-Grooming Development in the Rat. Physiology and Behavior, 50, 567-572. https://doi.org/10.1016/0031-9384(91)90547-2
Gramsbergen, A. and Westerga, J. (1992) Locomotor Development in Undernourished Rats. Behavioral Brain Research, 48, 57-64. https://doi.org/10.1016/S0166-4328(05)80139-1
Warr, W.B. and Guinan, J.J. (1979) Efferent Innervation of the Organ of Corti: Two Separate Systems. Brain Research, 173, 152-155. https://doi.org/10.1016/0006-8993(79)91104-1
White, J.S. and Warr, B.W (1983) The Dual Origins of the Olivocochlear Bundle in the Albino Rat. Journal of Comparative Neurology, 219, 203-214. https://doi.org/10.1002/cne.902190206
Aschoff, A. and Ostwald, J. (1988) Distribution of Cochlear Efferents and Olivocollicular Neurons in the Brainstem of the Rat and Guinea Pig. Experimental Brain Research, 71, 241-251. https://doi.org/10.1007/BF00247484
Carlier, E. and Pujol, R. (1978) Role of Inner and Outer Hair Cells in Coding Sound Intensity: An Ontogenetic Approach. Brain Research, 147, 174-176. https://doi.org/10.1016/0006-8993(78)90784-9
Ciuman, R.R. (2010) The Efferent System or Olivocochlear Function Bundle-Fine Regulator and Protector of Hearing Perception. International Journal Biomedical Sciences, 6, 276-288.
Salas, M., Torrero, C., Regalado, M., Martínez-Gómez, M. and Pacheco, P. (1994) Dendritic Arbor Alterations in the Medial Superior Olivary Neurons of Neonatally Underfed Rats. Acta Anatomica, 151, 180-187. https://doi.org/10.1159/000147661
Chen, Ch.Ch., Lu, J. and Zuo, Y. (2014) Spatiotemporal Dynamics of Dendritic Spines in the Living Brain. Frontiers in Neuroanatomy, 8, Article No. 28. https://doi.org/10.3389/fnana.2014.00028
Mansour, Y., Burchell, A. and Kulesza, R.J. (2021) Central Auditory and Vestibular Dysfunction Are Key Features of Autism Spectrum Disorder. Frontiers in Integrative Neuroscience, 15, Article ID: 743561. https://doi.org/10.3389/fnint.2021.743561
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. https://doi.org/10.1016/0378-5955(93)90113-F
Sima, A. and Sourander, P. (1978) The Effect of Pre- and Postnatal Undernutrition on Axonal Growth and Myelination of Central Motor Fibers. A Morphometric Study on Rat Cortico-Spinal Tract. Acta Neuropathologica, 4, 15-18. https://doi.org/10.1007/BF01273261
Rose, G.H. and Lindsley, D.B. (1968) Development of Visually Evoked Potentials in Kittens: Specific and Nonspecific Responses. Journal of Neurophysiology, 3, 607-623. https://doi.org/10.1152/jn.1968.31.4.607
Krigman, M.R. and Hogan, E.L. (1976) Undernutrition in the Developing Rat: Effect upon Myelination. Brain Research, 107, 239-255. https://doi.org/10.1016/0006-8993(76)90224-9
Olivares, R., Soto-Moyano, R., Hernández, A. and Aboitiz, F. (2002) La malnutrición prenatal proteica leve afecta el desarrollo del cuerpo calloso anterior. Revista Chilena de Anatomía, 20, 159-163. https://doi.org/10.4067/S0716-98682002000200007
Forbes, W., Stern, W., Tracy, C. and Resnick, G. (1978) Effect of Chronic Protein Malnutrition on Experimentally Induced Seizures in the Rat. Experimental Neurology, 62, 475-481. https://doi.org/10.1016/0014-4886(78)90069-9
Slotnick, B. (1967) Disturbance of Maternal Behavior in the Rat Following Lesions of the Cingulate Cortex. Behaviour, 29, 204-236. https://doi.org/10.1163/156853967X00127
Passetti, F., Chudasama, Y. and Robbins, T.W. (2002) The Frontal Cortex of the Rat and Visual Attentional Performance: Dissociable Functions of Distinct Medial Prefrontal Subregions. Cerebral Cortex, 12, 1254-1268. https://doi.org/10.1093/cercor/12.12.1254
Salas, M. and Cintra L. (1975) Development of the Electrocorticogram during Starvation in the Rat. Physiology and Behavior, 14, 589-593. https://doi.org/10.1016/0031-9384(75)90186-9
Malmierca, M.S. and Merchan, M.A. (2002) The Rat Auditory System. 4th Edition, Elsevier, Amsterdam, 1-55.
Sherman, S.M. and Guillery, R.W. (2011) Distinct Functions for Direct and Transthalamic Corticocortical Connections. Journal of Neurophysiology, 106, 1068-1077. https://doi.org/10.1152/jn.00429.2011
Rushmore, R.J., McGaughy, J.A., Amaral, A.C., Mokler, D.J., Morgane, P.J., Galler, J.R. and Rosene, D.L. (2021) The Neural Basis of Attentional Alterations in Prenatally Protein Malnourished Rats. Cerebral Cortex, 31, 497-512. https://doi.org/10.1093/cercor/bhaa239
Fukuda, Y. and Iwama, K. (1971) Reticular Inhibition of Internuncial Cells in the Rat Lateral Geniculate Body. Brain Research, 35, 107-118. https://doi.org/10.1016/0006-8993(71)90597-X
Hale, P.T., Sefton, A.J., Baur, L.A. and Cottee, L.J. (1982) Interrelations of the Rat’s Thalamic Reticular and Dorsal Lateral Geniculate Nuclei. Experimental Brain Research, 45, 217-229. https://doi.org/10.1007/BF00235781
Salas, M., Torrero, C. and Pulido, S. (1986) Undernutrition Induced by Early Pup Separation Delays the Development of the Thalamic Reticular Nucleus in Rats. Experimental Neurology, 93, 447-455. https://doi.org/10.1016/0014-4886(86)90166-4
Panksepp, J. and Biven, L. (2012) Ancestral Passions. In: Panksepp, J. and Biven, L., Eds., The Archaeology of Mind, W.W. Norton & Company, New York, Chapter 1, 11-12.
Kelly, J. and Hearing, P. (1996) Principles of Neural Science. 3rd Edition, Kandel, E.R., Schwartz, J.H. and Jessell, T.M., Eds., Appleton & Lange, Norwalk, 481-499.
Guétin, S., Giniés, P., Siou, D.K., Picot, M.C., Pommié, C., Guldner, E., Gosp, A.M., Ostyn, K., Coudeyre, E. and Touchon, J. (2012) The Effects of Music Intervention in the Management of Chronic Pain. A Single-Blind, Randomized, Controlled Trial. The Clinical Journal of Pain, 28, 329-337. https://doi.org/10.1097/AJP.0b013e31822be973
Angulo-Perkins, A., Aubé, W., Paretz, I., Barrios, F.A., Armony, J.L. and Concha, L. (2014) Music Listening Engages Specific Cortical Regions within the Temporal Lobes: Differences between Musicians and Non-Musicians. Cortex, 59, 126-137. https://doi.org/10.1016/j.cortex.2014.07.013
Torrero, C., Regalado, M., Rubio, L. and Salas, M. (2014) Effects of Neonatal Undernutrition on Development of the Dorsolateral Prefrontal Cortex Pyramidal Cells in the Rat. Journal of Behavioral and Brain Science, 4, 49-57. https://doi.org/10.4236/jbbs.2014.41007
Tonkiss, J., Galler, J.R., Shukitt-Hale, B. and Rocco, F.J. (1991) Prenatal Protein Malnutrition Impairs Visual Discrimination Learning in Adult Rats. Psychobiology, 19, 247-250. https://doi.org/10.3758/BF03332075
Numan, M., Bress, J.A., Ranker, L.R., Gary A.J., DeNicola, A.L., Bettis, J.K. and Knapp, S.E. (2010) The Importance of the Basolateral/Basomedial Amygdala for Goal-Directed Maternal Responses in Postpartum Rats. Behavioural Brain Research, 214, 368-376. https://doi.org/10.1016/j.bbr.2010.06.006
Chavez, C.M., McGaugh, J.L. and Weinberger, N.M. (2013) Activation of the Basolateral Amygdala Induces Long-Term Enhancement of Specific Memory Representations in the Cerebral Cortex. Neurobiology of Learning and Memory, 101, 8-18. https://doi.org/10.1016/j.nlm.2012.12.013
Sun, W., Zhang, L., Lu, J., Yang, G., Laundrie, E. and Salvi, R. (2008) Noise Exposure-Induced Enhancement of Auditory Cortex Response and Changes in Gene Expression. Neuroscience, 156, 374-380. https://doi.org/10.1016/j.neuroscience.2008.07.040
Rybalko, N., Mitrovic, D., Suta, D., Bures, Z., Popelár, J. and Syka, J. (2019) Behavioral Evaluation of Auditory Function Abnormalities in Adult Rats with Normal Hearing Thresholds That Were Exposed to Noise during Early Development. Physiology and Behavior, 210, Article ID: 112620. https://doi.org/10.1016/j.physbeh.2019.112620
Xerri, C., Coq, J.O., Merzenich, M.M. and Jenkins, W.M. (1996) Experience-Induced Plasticity of Cutaneous Maps in the Primary Somatosensory Cortex of Adult Monkeys and Rats. Journal of Physiology (Paris), 90, 277-287. https://doi.org/10.1016/S0928-4257(97)81438-6
Jordan, T.C., Cane, S.E. and Howells, K.F. (1981) Deficits in Spatial Memory Performance Induced by Early Undernutrition. Developmental Psychobiology, 14, 317-325. https://doi.org/10.1002/dev.420140404
Jordan, T.C., Howells, K.F., McNaughton, N. and Heatlie, P.L. (1982) Effects of Early Undernutrition on Hippocampal Development and Function. Research in Experimental Medicine, 180, 201-207. https://doi.org/10.1007/BF01852291
Andrade, J.P., Madeira, M.D. and Paula-Barbosa, M.M. (1995) Effects of Long-Term Malnutrition and Rehabilitation on the Hippocampal Formation of the Adult Rat. A Morphometric Study. Journal of Anatomy, 187, 379-393.
Jordan, T.C. and Clark, G.A. (1983) Early Undernutrition Impairs Hippocampal Long-Term Potentiation in Adult Rats. Behavioral Neuroscience, 97, 319-322. https://doi.org/10.1037/0735-7044.97.2.319
Diaz-Cintra, S., Cintra, L., Galvan, A., Aguilar, A., Kemper, T. and Morgane, P.J. (1991) Effects of Prenatal Protein Deprivation on Postnatal Development of Granule Cells in the Fascia Dentata. Journal of Comparative Neurology, 310, 356-364. https://doi.org/10.1002/cne.903100306
Franková, S. (1973) Effect of Chronic Protein-Calorie Malnutrition on the Development of Social Behavior in Rats. Developmental Psychobiology, 6, 33-43. https://doi.org/10.1002/dev.420060106
Wolf, C., Almli, C.R., Finger, S., Ryan, S. and Morgane, P.J. (1986) Behavioral Effects of Severe and Moderate Early Malnutrition. Physiology and Behavior, 38, 725-730. https://doi.org/10.1016/0031-9384(86)90270-2
Wiener, S.G., Robinson, L. and Levine, S. (1983) Influence of Perinatal Malnutrition on Adult Physiological and Behavioral Reactivity in Rats. Physiology and Behavior, 30, 41-50. https://doi.org/10.1016/0031-9384(83)90036-7
Walker, C.D. and Aubert, M.L. (1988) Effects of Early Undernutrition and Handling on the Adrenocortical Activity of Neonatal Rats. Life Sciences, 43, 1983-1990. https://doi.org/10.1016/0024-3205(88)90571-1
Escobar, C. and Salas, M. (1993) Neonatal Undernutrition and Amygdaloid Nuclear Complex Development: An Experimental Study in the Rat. Experimental Neurology, 122, 311-318. https://doi.org/10.1006/exnr.1993.1130
Kraus, K.S. and Canlon, B. (2012) Neuronal Connectivity and Interactions between the Auditory and Limbic Systems. Effects of Noise and Tinnitus. Hearing Research, 288, 34-46. https://doi.org/10.1016/j.heares.2012.02.009
Aizenberg, M., Rolon-Martinez, S., Pham, T., Rao, W., Haas, J.S. and Geffen, M.N. (2019) Projection from the Amygdala to the Thalamic Reticular Nucleus Amplifies Cortical Sound Responses. Cell Reports, 28, 605-615.E4. https://doi.org/10.1016/j.celrep.2019.06.050
Liston, C., Miller, M.M., Goldwater, D.S., Radley, J.J., Rocher, A.B., Hof, P.R., Morrion, J.H. and McEwen, B.S. (2006) Stress-Induced Alterations in Prefrontal Cortical Dendritic Morphology Predicts Selective Impairments in Perceptual Attentional Set-Shifting. The Journal of Neuroscience, 26, 7870-7874. https://doi.org/10.1523/JNEUROSCI.1184-06.2006
Febo, M., Stolberg, T.I., Numan, M., Bridges, R.S., Kulkami, P. and Ferris, C.F. (2008) Nursing Stimulation Is More than Tactile Sensation: It Is a Multisensory Experience. Hormones and Behavior, 54, 330-339. https://doi.org/10.1016/j.yhbeh.2008.02.024
Blood, A.J. and Zatorre, R.J. (2001) Intensely Pleasurable Responses to Music Correlate with Activity in Brain Regions Implicated in Reward and Emotion. Proceedings of the National Academy of Sciences of the United States of America, 98, 11818-11823. https://doi.org/10.1073/pnas.191355898
Reppucci, Ch.J. and Petrovich, G.D. (2016) Organization of Connections between the Amygdala, Medial Prefrontal Cortex, and Lateral Hypothalamus: A Single and Double Retrograde Tracing Study in Rats. Brain Structure and Function, 221, 2937-2962. https://doi.org/10.1007/s00429-015-1081-0
Fleming, A.S., O’Day, D.H. and Kraemer, G.W. (1999) Neurobiology of Mother-Infant Interactions: Experience and Central Nervous System Plasticity across Development and Generations. Neuroscience and Biobehavioral Reviews, 23, 673-685. https://doi.org/10.1016/S0149-7634(99)00011-1
Brudzynski, S.M., Kehoe, P. and Callaham, M. (1999) Sonographic Structure of Isolation-Induced Ultrasonic Calls of Rat Pups. Developmental Psychobiology, 34, 195-204. https://doi.org/10.1002/(SICI)1098-2302(199904)34:3 3.0.CO;2-S
Brachi, I., Santucci, D. and Alleva, E. (2006) Analysis of Ultrasonic Vocalizations Emitted by Infant Rodents. Current Protocols in Toxicology, 30, 13.12.1-13.12.14. https://doi.org/10.1002/0471140856.tx1312s30
Sawczuk, A. and Mosier, K.M. (2001) Neural Control of Tongue Movement with Respect to Respiration and Swallowing. Critical Reviews in Oral Biology and Medicine, 12, 18-37. https://doi.org/10.1177/10454411010120010101
Riede, T. (2011) Subglottal Pressure, Tracheal Airflow, and Intrinsic Laryngeal Muscle Activity during Rat Ultrasound Vocalization. Journal of Neurophysiology, 106, 2580-2592. https://doi.org/10.1152/jn.00478.2011
Patrickson, J.W., Smith, T E. and Zhou, S.S. (1991) Afferent Projections of the Superior and Recurrent Laryngeal Nerves. Brain Research, 539, 169-174. https://doi.org/10.1016/0006-8993(91)90702-W
Pascual-Font, A., Hernandez-Morato, I., McHanwell, S., Vazquez, T., Maranillo, E., Sañudo, J. and Valderrama-Canales, F.J. (2011) The Central Projections of the Laryngeal Nerves in the Rat. Journal of Anatomy, 219, 217-228. https://doi.org/10.1111/j.1469-7580.2011.01390.x
Pires-De-Melo, I.H., Wanderley Dos Reis, F., Luz, L.S., Paz, S.T., Silva, H.J., Souza, S.L. and Leandro, C.G. (2009) Short and Long-Term Effects of a Neonatal Low- Protein Diet in Rats on the Morphology of the Larynx. Nutrition, 25, 855-860. https://doi.org/10.1016/j.nut.2008.12.015
López-Jimenez, D., Torrero, C., Regalado, M. and Salas, M. (2013) Effects of Perinatal Undernutrition and Massage Stimulation upon the Ambiguous Nucleus in the Rat Prior to Weaning. Journal of Behavioral and Brain Sciences, 3, 200-209. https://doi.org/10.4236/jbbs.2013.32021
Smart, J.L. (1976) Maternal Behavior of Undernourished Mother Rats towards Well Fed and Underfed Young. Physiology and Behavior, 16, 147-149. https://doi.org/10.1016/0031-9384(76)90298-5
Moriceau, S. and Sullivan, R.M. (2006) Maternal Presence Serves as a Switch between Learning Fear and Attraction in Infancy. Nature Neuroscience, 9, 1004-1006. https://doi.org/10.1038/nn1733
Murmu, M.S., Salomon, S., Biala, Y., Weinstock, M., Braun, K. and Bock, J. (2006) Changes of Spine Density and Dendritic Complexity in the Prefrontal Cortex in Offspring of Mothers Exposed to Stress during Pregnancy. European Journal of Neuroscience, 24, 1477-1487. https://doi.org/10.1111/j.1460-9568.2006.05024.x
Rubio, L., Torrero, C., Regalado, M. and Salas, M. (2004) Alterations in the Solitary Tract Nucleus of the Rat Following Perinatal Food Restriction and Subsequent Nutritional Rehabilitation. Nutritional Neuroscience, 7, 291-300. https://doi.org/10.1080/10284150400019922
Frias, C., Torrero, C., Regalado, M. and Salas, M. (2006) Organization of Olfactory Glomeruli in Neonatally Undernourished Rats. Nutritional Neuroscience, 9, 49-55. https://doi.org/10.1080/10284150500506042
Ochelli, V., Spence, C. and Zampini, M. (2011) Audiotactile Interactions in Temporal Perception. Psychonomic Bulletin Review, 18, 429-454. https://doi.org/10.3758/s13423-011-0070-4
Torrero, C., Regalado, M., Perez, E., Rubio, L. and Salas, M. (2005) Neonatal Food Restriction and Binaural Ear Occlusion Interfere with the Maturation of Cortical Motor Pyramids in the Rat. Nutritional Neuroscience, 8, 63-66. https://doi.org/10.1080/10284150400027131
Arroyo-Anlló, E.M., Dauphin, S., Fargeau, M.N., Ingrand, P. and Gil, R. (2019) Music and Emotion in Alzheimer’s Disease. Alzheimer’s Research and Therapy, 11, Article No. 69. https://doi.org/10.1186/s13195-019-0523-y