Sweet and Bitter Tastes Evoked Different Neuronal Activation in the Rostral Portion of the Nucleus of the Solitary Tract of Developing Rats

Abstract

The impact of the gustatory stimuli on the rostral portion of the nucleus of the solitary tract (rNST) was investigated in developing rats, by using c-fos immunohistochemical staining. Wistar male rats of 5, 15, and 25 days of age were isolated from the mother for 12 h, then stimulated via the intraoral route with quinine, sucrose, or NaCl, and sacrificed 90 min later. The water-stimulated group showed minimal c-fos-like immunoreactivity (FLI) compared with taste-stimulated groups that exhibited different FLI in the rNST at the different ages. At all ages the quinine-stimulated group induced FLI in the medial subfield, while sucrose induced FLI in the lateral subfield of the rNST. The intensity of FLI was highest at P15, and it declined at P25. These findings provide detailed insight into the anatomical basis of rNST activation that is involved in early food intake and the learning capacity of the newborn.

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L. Rubio-Navarro, C. Torrero, M. Regalado and M. Salas, "Sweet and Bitter Tastes Evoked Different Neuronal Activation in the Rostral Portion of the Nucleus of the Solitary Tract of Developing Rats," Journal of Behavioral and Brain Science, Vol. 2 No. 3, 2012, pp. 291-298. doi: 10.4236/jbbs.2012.23033.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] J. M. Cernoch and R. H. Porter, “Recognition of Maternal Axillary Odors by Infants,” Child Development, Vol. 56, No. 6, 1985, pp. 1593-1598. doi:10.2307/1130478
[2] 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
[3] I. Farbman “Electron Microscope Study of the Developing Taste Bud in Rat Fungiform Papilla,” Developmental Biology, Vol. 11, No. 1, 1965, pp. 110-135. doi:10.1016/0012-1606(65)90040-0
[4] M. Mistreta, “Topographic and Histological Study of the Developing Rat Tongue, Palate and Taste Buds,” In: J. F. Bosma, Ed., Third Symposium on Oral Sensations and Perception, I. L: Charles, C. Thomas, Springfield, 1972, pp. 163-187.
[5] J. P. Mbiene and A. I. Farbman, “Evidence for Stimulus Access to Taste Cells and Nerves during Development: An Electron Microscopic Study,” Microscopy Research and Technique, Vol. 26, No. 2, 1993, pp. 94-105. doi:10.1002/jemt.1070260203
[6] M. A. Hosley and B. Oskley, “Postnatal Development of the Vallate Papilla and Taste Buds in Rats,” The Anatomical Record, Vol. 218, No. 2, 1987, pp. 216-222. doi:10.1002/ar.1092180217
[7] R. F. Krimm and D. L. Hill, “Innervation of Single Fungiform Taste Buds during Development in Rat,” The Journal of Comparative Neurology, Vol. 398, No. 1, 1998, pp. 13-24. doi:10.1002/(SICI)1096-9861(19980817)398:1<13::AID-CNE2>3.0.CO;2-C
[8] P. S. Lasiter, D. M. Wong and D. L Kachele, “Postnatal Development of the Rostral Solitary Nucleus in Rat: Dendritic Morphology and Mitochondrial Enzyme Activity,” Brain Research Bulletin, Vol. 22, No. 2, 1989, pp. 313-321. doi:10.1016/0361-9230(89)90059-2
[9] P. S. Lasiter and D. L. Kachele, “Elevated NADH-Dehydrogenase Activity Characterizes the Rostral Gustatory Zone of the Solitary Nucleus in Rat,” Brain Research Bulletin, 1989, Vol. 22, No. 4, pp. 777-781. doi:10.1016/0361-9230(89)90099-3
[10] 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
[11] H. Bao, R. M. Bradley and C. M. Mistretta, “Development of Intrinsic Electrophysiological Properties in Neurons from the Gustatory Region of Rat Nucleus of Solitary Tract,” Developmental Brain Research, Vol. 86, No. 1-2, 1995, pp. 143-154. doi:10.1016/0165-3806(95)00020-E
[12] M. Mistretta and S. Labyak, “Maturation of Neuron Types in Nucleus of Solitary Tract Associated with Functional Convergence during Development of Taste Circuits,” The Journal of Comparative Neurology, Vol. 345, No. 3, 1994, pp. 359-376. doi:10.1002/cne.903450304
[13] W. E. Renehan, J. Massey, Z. Jin, X. Zhang, Z. Liu and L. Schweitzer, “Developmental Changes in the Dendritic Architecture of Salt-Sensitive Neurons in the Nucleus of the Solitary Tract,” Developmental Brain Research, Vol. 102, No. 2, 1997, pp. 231-246. doi:10.1016/S0165-3806(97)00104-1
[14] A. Vincent and F. Tell, “Postnatal Development of Rat Nucleus Tractus Solitarius Neurons: Morphological and Electrophysiological Evidence,” Neuroscience, Vol. 93, No. 1, 1999, pp. 293-305. doi:10.1016/S0306-4522(99)00109-8
[15] M. I. Harrer and S. P. Travers, “Topographic Organization of Fos-Like Immunoreactivity in the Rostral Nucleus of the Solitary Tract Evoked by Gustatory Stimulation with Sucrose and Quinine,” Brain Research, Vol. 11, No. 1-2, 1996, pp. 125-137. doi:10.1016/0006-8993(95)01410-1
[16] S. P. Travers and H. Hu, “Extranuclear Projections of rNST Neurons Expressing Gustatory-Elicited Fos,” The Journal of Comparative Neurology, Vol. 427, No. 1, 2000, pp. 124-138. doi:10.1002/1096-9861(20001106)427:1<124::AID-CNE8>3.0.CO;2-2
[17] S. P. Travers, “Quinine and Citric Acid Elicit Distinctive Fos-Like Immunoreactivity in the Nucleus of the Solitary Tract,” American Journal of Physiology, Vol. 282, No. 6, 2002, pp. 1798-1810.
[18] J. R. Ganchrow, J. E. Steiner and S. Canetto, “Behavioral Displays to Gustatory Stimuli in Newborn Rat Pups,” Developmental Psychobiology, Vol. 19, No. 3, 1986, pp. 163-174. doi:10.1002/dev.420190303
[19] G. J. Shwartz and H. J. Grill, “Comparing Taste-Elicited Behaviors in Adult and Neonatal Rats,” Appetite, Vol. 6, No.4, 1985, pp. 373-386. doi:10.1016/S0195-6663(85)80005-2
[20] B. Johanson and E. G. Shapiro, “Intake and Behavioral Responsiveness to Taste Stimuli in Infant Rats from 1 to 15 Days of Age,” Developmental Psychobiology, Vol. 19, No. 6, 1986, pp. 593-606. doi:10.1002/dev.420190610
[21] W. G. Hall and T. E. Bryan, “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 and Physiological Psychology, Vol. 95, No. 2, 1981, pp. 240-251. doi:10.1037/h0077771
[22] M. Sagar, F. R. Sharp and T. Currant, “Expression of c-Fos Protein in Brain: Metabolic Mapping at the Cellular Level,” Science, Vol. 240, No. 4857, 1988, pp. 1328-1331. doi:10.1126/science.3131879
[23] L. A. DiNardo and J. B. Travers, “Distribution of Fos-Like Immunoreactivity in the Medullary Reticular Formation of the Rat after Gustatory Elicited Ingestion and rejection Behaviors,” The Journal of Neuroscience, Vol. 17, No. 10, 1997, pp. 3826-3839.
[24] C. T. King, S. P. Travers, N. E. Rowland, M. Garcea and A. C. Spector, “Glossopharyngeal Nerve Transection Eliminates Quinine-Stimulated Fos-Like Immunoreactivity in the Nucleus of the Solitary Tract: Implications for a Functional Topography of Gustatory Nerve Input in Rats,” The Journal of Neuroscience, Vol. 19, No. 8, 1999, pp. 3107-3121.
[25] S. M. Altshuler, X. Bao, D. Bieger, D. A. Hopkins and R. R. Miselis, “Viscerotopic Representation of the Upper Alimentary Tract in the Rat: Sensory Ganglia and Nuclei of the Solitary and Spinal Trigeminal Tracts,” The Journal of Comparative Neurology, Vol. 283, No. 2, 1989, pp. 248-268. doi:10.1002/cne.902830207
[26] T. Morales, L. Aguilar, E. Ramos, F. Mena and C. Morgan, “Fos Expression Induced by Milk Ingestion in the Caudal Brainstem of Neonatal Rats,” Brain Research, Vol. 1241, No. 19, 2008, pp. 76-83. doi:10.1016/j.brainres.2008.09.022
[27] G. Paxinos, K. W. S. Ashwell and I. Tork, “Atlas of the Developing Rat Nervous System,” 2nd Edition, Academic Press, Waltham, 1994.
[28] G. Paxinos and C. Watson, “The Rat Brain in Stereotaxic Coordinates,” Academic Press, Waltham, 1997.
[29] S. S. Miller and N. E. Spear, “Olfactory Learning in the Rat Neonate Soon after Birth,” Developmental Psychobiology, Vol. 50, No. 6, 2008, pp. 554-565. doi:10.1002/dev.20318
[30] D. Hill and C. R. Almil, “Ontogeny of Chorda Tympani Nerve Responses to Gustatory Stimuli in the Rat,” Brain Research, Vol. 197, No. 1, 1980, pp. 27-38. doi:10.1016/0006-8993(80)90432-1
[31] D. Hill, R. M. Bradley and C. M. Mistretta, “Development of Taste Responses in the Rat Nucleus of Solitary Tract,” Journal of Neurophysiology, Vol. 50, No. 4, 1983, pp. 879-895.
[32] D. M. Wong and D. L. Kachele, “Postnatal Development of the Rostral Solitary Nucleus in Rat: Dendritic Morphology and Mitochondrial Enzyme Activity,” Brain Research Bulletin, Vol. 22, No. 2, 1989, pp. 313-321. doi:10.1016/0361-9230(89)90059-2
[33] P. S. Lasiter, “Postnatal Development of Gustatory Recipient Zones within the Nucleus of the Solitary Tract,” Brain Research Bulletin, Vol. 28, No. 5, 1992, pp. 667-677. doi:10.1016/0361-9230(92)90245-S
[34] A. K. Thaw, S. Frakmann and D. L. Hill, “Behavioral Taste Responses of Developmentally NaCl-Restricted Rats to Various Concentrations of NaCl,” Behavioral Neuroscience, Vol. 114, No. 2, 2000, pp. 437-441. doi:10.1037/0735-7044.114.2.437
[35] O. May and D. Hill, “Gustatory Terminal Field Organization and Developmental Plasticity in the Nucleus of the Solitary Tract Revealed through Triple-Fluorescence Labeling,” The Journal of Comparative Neurology, Vol. 497, No. 4, 2006, pp. 658-669. doi:10.1002/cne.21023
[36] J. Mangold and D. Hill, “Postnatal Reorganization of Primary Afferent Terminal Fields in the Rat Gustatory Brainstem Is Determined by Prenatal Dietary History,” The Journal of Comparative Neurology, Vol. 509, No. 6, 2008, pp. 594-607. doi:10.1002/cne.21760
[37] J. E. Steiner and D. Glaser, “Differential Behavioural Responses to Taste Stimuli in Non-Human Primates,” Journal of Human Evolution, Vol. 13, No. 8, 1984, pp. 709-723. doi:10.1016/S0047-2484(84)80021-4
[38] J. E. Steiner, “Human Facial Expressions in Response to Taste and Smell Stimulation,” In: R. W. Hayne and L. P. Lipsitt, Eds., Advance in Child Development and Behavior, Academic Press, Inc., New York, 1979, pp. 257-293.
[39] S. P. Travers and J. B. Travers, “Reflex Topography in the Nucleus of the Solitary Tract,” Chemical Senses, Vol. 30, No. 1, 2005, pp. 180-181. doi:10.1093/chemse/bjh173
[40] M. C. Whitehead, “Neuroanatomy of the Gustatory System,” Gerodontics, Vol. 5, No. 5, 1988, pp. 239-243.
[41] T. Hanamori and N. Oshiko, “Cardiovascular Responses to Gustatory and Mechanical Stimulation of the Nasopharynx in Rats,” Brain Research, Vol. 619, No. 1-2, 1993, pp. 214-222. doi:10.1016/0006-8993(93)91614-X
[42] T. Yamamoto and K. Sawa, “c-Fos like Immunoreactivity in the Brainstem Following Intraoral and Intragastrica Infusion of Chemical Solutions in Rats”, Brain Research, Vol. 866, No. 1-2, 2000, pp. 144-151. doi:10.1016/S0006-8993(00)02242-3
[43] H. Ogawa, T. Imoto and T. Hayama, “Responsiveness of Solitario-Parabrachial Relay Neurons to Taste and Mechanical Stimulation Applied to the Oral Cavity in Rats,” Experimental Brain Research, Vol. 54, No. 2, 1984, pp. 349-358.
[44] S. P. Travers and R. Norgren, “Organization of Orosensory Responses in the Nucleus of the Solitary Tract of the Rat,” Journal of Neurophysiology, Vol. 73, No. 6, 1995, pp. 2144-2162.
[45] E. Erkadius, T. O. Morgan and R. Di Nico, “Aminiotic Fluid Composition and Fetal and Placental Growth Rates in Genetically Hypertensive and Normotensive Rats,” Reproduction, Fertility and Development, Vol. 7, No. 6, 1995, pp. 1563-1567. doi:10.1071/RD9951563
[46] R. Hudson and H. Distel, “The Flavour of Life: Perinatal Development of Odour and Taste Preferences,” Schweizerische Medizinische Wochenschrift, Vol. 129, No. 5, 1999, pp. 176-181.
[47] M. Dragunow and R. Fall, “The Use of c-Fos as a Metabolic Marker in Neuronal Pathway Tracing,” Journal of Neuroscience Methods, Vol. 29, No. 3, 1989, pp. 261-265. doi:10.1016/0165-0270(89)90150-7
[48] M. Sheng and M. E. Greenberg, “The Regulation and Function of c-Fos and Other Immediate Early Genes in the Nervous System,” Neuron, Vol. 4, No. 4, 1990, pp. 477-485. doi:10.1016/0896-6273(90)90106-P
[49] J. I. Morgan and T. Currant, “Stimulus-Transcription Coupling in the Nervous System: Involvement of the Inducible Proto-Oncogenes Fos and jun,” Annual Review Neuroscience, Vol. 14, No. 1, 1991, pp. 421-451. doi:10.1146/annurev.ne.14.030191.002225
[50] L. Kaczmarek and A. Chaudhuri, “Sensory Regulation of Immediate-Early Gene Expression in Mammalian Visual Cortex: Implications for Functional Mapping and Neural Plasticity,” Brain Research Reviews, Vol. 23, No. 3, 1997, pp. 237-256. doi:10.1016/S0165-0173(97)00005-2
[51] R. Wickstrom, T. Hokfelt and H. Lagererantz, “Development of CO2-Responses in the Early Newborn Period in Rat,” Respiratory Physiology & Neurobiology, Vol. 132, No. 2, 2002, pp. 145-158. doi:10.1016/S1569-9048(02)00076-9
[52] K. M. Guthrie and C. Gall, “Anatomic Mapping of Neuronal Odor Responses in the Developing Rat Olfactory Bulb,” The Journal of Comparative Neurology, Vol. 455, No. 1, 2003, pp. 56-71. doi:10.1002/cne.10452

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