Analysis of the Sensory and Hedonic Impacts of Sweet and Bitter Tastes in Perinatally Underfed Rats

Abstract

Newborn rats discriminate tastes and generate gustofacial response (GFR) because the neuronal substrate is already operating. The oral application of sucrose or quinine hydrochloride produces a specific GFR. We analyzed the effects of perinatal undernutrition on the GFR development of rats at two cue concentrations. In the undernourished group, pregnant dams received different percentages of a balance diet. After birth, prenatally underfed pups continue the undernourishment by remaining for 12 h with a foster dam, and for 12 h with a nipple-ligated mother. Cues were presented as a single droplet of sucrose, sodium chloride, or quinine at low or high concentrations onto the lips at postnatal days (PDs) 1 and 3, and mouth-opening (MOF) and lip-licking frequencies (LLF) were noted. On PD 1 the undernourished group showed smaller MOF increases in response to low salt and quinine stimuli than the controls but no differences at high concentrations. On PD 3, both low and high concentrations of the sucrose and quinine cues significantly increased the MOF in the underfed compared to the control group. Low but not high salt decreased LLF on PD1 in the underfed compared to the control group. On PD 3 the undernourished pups showed significant increases of LLF with low quinine compared with the control rats, but the reverse was observed with high quinine. These data suggest that perinatal undernutrition affects the development of the sensory and hedonic aspects of taste causing changes in GFR expression.

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Rubio-Navarro, L. , Torrero, C. , Regalado, M. and Salas, M. (2014) Analysis of the Sensory and Hedonic Impacts of Sweet and Bitter Tastes in Perinatally Underfed Rats. Journal of Behavioral and Brain Science, 4, 423-431. doi: 10.4236/jbbs.2014.49041.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Grill, H.J. and Norgren, R. (1978) The Taste Reactivity Test. I. Mimetic Responses to Gustatory Stimuli in Neurologically Normal Rats. Brain Research, 143, 263-279.
[2] Kinzeler, N.R. and Travers, S.P. (2008) Licking and Gaping Elicited by Microstimulation of the Nucleus of the Solitary Tract. American Journal of Physiology Regulatory Integrative Comparative Physiology, 295, R436-448.
http://dx.doi.org/10.1152/ajpregu.00189.2008
[3] Steiner, J.E. (1974) Innate Discriminative Human Facial Expression to Taste and Smell Stimulation. Annals of the New York Academies of Science, 237, 229-233.
http://dx.doi.org/10.1111/j.1749-6632.1974.tb49858.x
[4] Yamamoto, T., Matsuo, R., Fujiwara, T. and Kawamura, Y. (1982) EMG Activities of Masticatory Muscles during Licking in Rats. Physiology and Behavior, 29, 905-913.
http://dx.doi.org/10.1016/0031-9384(82)90342-0
[5] Berridge, K.C. (2000) Taste Reactivity: Measuring Hedonic Impact in Human Infants and Animals. Neuroscience Bio-behavioral Review, 24, 173-198.
http://dx.doi.org/10.1016/S0149-7634(99)00072-X
[6] Steiner, J.E., Glaser, D., Hawilo, M.E. and Berridge, K.C. (2001) Comparative Expression of Hedonic Impact: Affective Reactions to Taste by Human Infants and other Primates. Neuroscience Biobehavioral Review, 25, 53-74.
http://dx.doi.org/10.1016/S0149-7634(00)00051-8
[7] Hladik, C.M. and Simmen, B. (1996) Taste Perception and Feeding Behavior in Nonhuman Primates and Human Populations. Evolutionary Anthropology, 5, 58-71.
http://dx.doi.org/10.1002/(SICI)1520-6505(1996)5:2<58::AID-EVAN5>3.0.CO;2-S
[8] Rozin, P. (1996) The Socio-Cultural Context of Eating and Food Choice. In: Meiselman, H.L. and MacFie, H.J.H., Eds., Food Choice, Acceptance and Consumption, Blackie Academic, London, 83-104.
http://dx.doi.org/10.1007/978-1-4613-1221-5_2
[9] Sewards, T.V. (2004) Dual Separate Pathways for Sensory and Hedonic Aspects of Taste. Brain Research Bulletin, 62, 271-283.
http://dx.doi.org/10.1016/j.brainresbull.2003.10.004
[10] Uenoa, A., Uenob, Y. and Tomonagac, M. (2004) Facial Responses to Four Basic Tastes in Newborn Rhesus Macaques. (Macaca mulatta) and Chimpanzees (Pan troglodytes). Behavioural Brain Research, 154, 261-271.
http://dx.doi.org/10.1016/j.bbr.2004.02.014
[11] Salas, M., Torrero, M.C., Regalado, M. and Rubio, L. (2012) Development of the Gusto Facial Reflex in Perinatally Undernourished Rats. Journal of Behavioral and Brain Science, 2, 308-314.
http://dx.doi.org/10.4236/jbbs.2012.23035
[12] Schwartz, G.J. and Grill, H.J. (1985) Comparing Taste-Elicited Behavior in Adult and Neonatal Rats. Appetite, 6, 373-386.
http://dx.doi.org/10.1016/S0195-6663(85)80005-2
[13] Johanson, I.B. and Shapiro, E.G. (1986) Intake and Behavioral Responsiveness to Taste Stimuli in Infant Rats from 1 to 15 Days of Age. Developmental Psychobiology, 19, 593-606.
http://dx.doi.org/10.1002/dev.420190610
[14] Mennella, J.A. (2014) Ontogeny of Taste Preferences: Basic Biology and Implications for Health. American Journal Clinical Nutrition, 99, 704S-711S.
http://dx.doi.org/10.3945/ajcn.113.067694
[15] Portella, A.K., Kajantie, E., Hovi, P., Desai, M., Ross, M.G., Goldani, M.Z., Rosenboom, T.J. and Silveira, P.P. (2012) Effects of in Utero Conditions on Adult Feeding Preferences. Journal of Developmental Origins of Health and Disease, 3, 140-152.
http://dx.doi.org/10.1017/S2040174412000062
[16] Torrero, C., Regalado, M., Rubio, L., Ruiz-Marcos, A. and Salas, M. (2003) Neonatal Food Restriction Induces Hypoplasia in Developing Facial Motor Neurons of Rats. Nutritional Neuroscience, 6, 317-324.
http://dx.doi.org/10.1080/10284150310001595618
[17] 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.
http://dx.doi.org/10.1080/10284150400019922
[18] Frias, C., Torrero, C., Regalado, M. and Salas, M. (2009) Development of Mitral Cells and Olfactory Bulb Layers in Neonatally Undernourished Rats. Nutritional Neuroscience, 12, 96-104.
http://dx.doi.org/10.1179/147683009X423238
[19] Salas, M., Torrero, C., Rubio, L. and Regalado, M. (2012) Effects of Perinatal Undernutrition on the Development of Neurons in the Rat Insular Cortex. Nutritional Neuroscience, 15, 20-25.
http://dx.doi.org/10.1179/1476830512Y.0000000014
[20] Salas, M., Torrero, C., Regalado, M. and Perez, E. (2002) Retrieving of Pups by Neonatally Stressed Mothers. Nutritional Neuroscience, 5, 399-405.
http://dx.doi.org/10.1080/1028415021000055943
[21] Loranca, A., Torrero, C. and Salas, M. (1999) Development of Play Behavior in Neonatally Undernourished Rats. Physiology and Behavior, 66, 3-10.
http://dx.doi.org/10.1016/S0031-9384(98)00235-2
[22] Vanderbergh, J.G. (2003) Prenatal Hormone Exposure and Sexual Variation. American Scientist, 91, 218-225.
http://dx.doi.org/10.1511/2003.3.218
[23] Lynch, A. (1976) Postnatal Undernutrition: An Alternative Method. Developmental Psychobiology, 9, 39-48.
http://dx.doi.org/10.1002/dev.420090107
[24] Crnic, S., Bell, J.M., Mangold, R., Gruenthal, M., Eiler, M.J. and Finger, S. (1981) Separation-Induced Early Malnutrition: Maternal, Physiological and Brain Effects. Physiology and Behavior, 26, 695-707.
http://dx.doi.org/10.1016/0031-9384(81)90147-5
[25] Van den Hove, D.L.A., Steinbusch, H.W., Scheepens, A., Van de Berg, W.D., Kooiman, L.A., Boosten, B.J., Prickaerts, J. and Blanco, C.E. (2006) Prenatal Stress and Neonatal Rat Brain Development. Neuroscience, 137, 145-155.
http://dx.doi.org/10.1016/j.neuroscience.2005.08.060
[26] Altman, J. and Bayer, S.A. (1980) Development of the Brain Stem in the Rat. II. Thymidine-Radiographic Study of the Time of Origin of Neurons of the Upper Medulla, Excluding the Vestibular and Auditory Nuclei. Journal of Comparative Neurology, 194, 37-56.
http://dx.doi.org/10.1002/cne.901940103
[27] Harada, S., Yamaguchi, K., Kanemaru, N. and Kasahara, Y. (2000) Maturation of Taste Buds on the Soft Palate of the Postnatal Rat. Physiology and Behavior, 68, 333-339.
http://dx.doi.org/10.1016/S0031-9384(99)00184-5
[28] Ganchrow, J.R., Steiner, J.E. and Canett, S. (1986) Behavioral Displays to Gustatory Stimuli in Newborn Rat Pups. Developmental Psychobiology, 19, 163-174.
http://dx.doi.org/10.1002/dev.420190303
[29] Hall, W.G. and Bryan, T.E. (1981) The Ontogeny of Feeding in Rats: IV. Taste Development as Measured by Intake and Behavioral Responses to Oral Infusions of Sucrose and Quinine. Journal of Comparative Physiological Psychology, 95, 240-251.
http://dx.doi.org/10.1037/h0077771
[30] McBurney, D.H. (1969) A Note on the Relation between Area and Intensity in Taste. Perception and Psychophysics, 6, 250.
http://dx.doi.org/10.3758/BF03207027
[31] Berridge, K.C. (1991) Modulation of Taste Affect by Hunger, Caloric Satiety, and Sensory-Specific Satiety in the Rat. Appetite, 16, 103-120.
http://dx.doi.org/10.1016/0195-6663(91)90036-R
[32] Doyle, T.G., Berridge, K.C. and Gosnell, B.A. (1993) Morphine Enhances Hedonic Taste Palatability in Rats. Pharmacology Biochemistry and Behavior, 46, 745-749.
http://dx.doi.org/10.1016/0091-3057(93)90572-B
[33] Travers, J.B., Dinardo, L.A. and Karimnamazi, H. (1997) Motor and Premotor Mechanisms of Licking. Neuroscience and Biobehavioral Review, 21, 631-647.
http://dx.doi.org/10.1016/S0149-7634(96)00045-0
[34] Nizhnikov, M.E., Varlinskaya, E.I., Petrov, E.S. and Spear, N.E. (2006) Reinforcing Properties of Ethanol in Neonatal Rats: Involvement of the Opioid System. Behavioral Neuroscience, 120, 267-280.
http://dx.doi.org/10.1037/0735-7044.120.2.267
[35] Sederholm, F. and Sodersten, P. (2001) Aversive Behavior during Intraoral Intake in Male Rats. Physiology and Behavior, 74, 153-168.
http://dx.doi.org/10.1016/S0031-9384(01)00534-0
[36] Greizerstei, H.B. (1982) Placental and Fetal Composition during the Last Trimester of Gestational in the Rat. Biology of Reproduction, 26, 847-853.
http://dx.doi.org/10.1095/biolreprod26.5.847
[37] Ghiaroni, V., Fieni, F., Pietra, P. and Bigiani, A. (2003) Electrophysiological Heterogeneity in a Functional Subset of Mouse Taste Cells during Postnatal Development. Chemical Senses, 28, 827-833.
http://dx.doi.org/10.1093/chemse/bjg076
[38] Salas, M., Pulido, M.S., Torrero, C. and Escobar, C. (1991) Neonatal Undernutrition and Self-Grooming Development in the Rat: Long-Term Effects. Physiology and Behavior, 50, 567-572.
http://dx.doi.org/10.1016/0031-9384(91)90547-2
[39] Colonnese, M.T., Stallman, E.L. and Berridge, K.C. (1996) Ontogeny of Action Syntax in Altricial and Precocial Rodents: Grooming Sequences by Rat and Guinea Pig Pups. Behaviour, 133, 1165-1195.
http://dx.doi.org/10.1163/156853996X00350
[40] Steiner, J.E. (1973) The Gustofacial Response: Observation on Normal and Anencephalic Newborn Infants. Symposium on Oral Sensation and Perception, 4, 254-278.
[41] Schambergh, S.M., Evoniuk, G.E. and Kuhn, C.M. (1984) Tactile and Nutritional Aspects of Maternal Care: Specific Regulators of Neuroendocrine Function and Cellular Development. Experimental Biology and Medicine, 175, 135-146. http://dx.doi.org/10.3181/00379727-175-41779
[42] Walker, C.D., Deschamps, S., Proulx, K., Tu, M., Salzman, C., Woodside, B., Lupien, S., Gallo-Payet, N. and Richard, D. (2004) Mother to Infant or Infant to Mother? Reciprocal Regulation of Responsiveness to Stress in Rodents and the Implications for Humans. Journal of Psychiatry & Neuroscience, 29, 364-382.

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