Vagal gustatory reflex circuits for intraoral food sorting behavior in the goldfish: Cellular organization and neurotransmitters

Journal of Comparative Neurology

Volumn 516, Issue 3, 2009, Pages 213-225

  Ikenaga, Takanori ^a,c   Ogura, Tatsuya ^a,b   Finger, Thomas E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^c UNIVERSITY OF HYOGO   (Japan)

Author keywords

Cyprinid fish; Glutamate; Gustatory; Nucleus solitary tract; Oro branchial reflex; Vagal lobe

Indexed keywords

AMPA RECEPTOR; BIOCYTIN; CALCIUM; GLUTAMIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMBIGUUS NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; DENDRITE; ELECTROSTIMULATION; FEEDING BEHAVIOR; FEMALE; GOLDFISH; GUSTATORY SYSTEM; HISTOLOGY; INTERNEURON; MALE; MOTONEURON; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SOLITARY TRACT NUCLEUS; TASTE BUD; VAGUS REFLEX;

ANIMALS; CALCIUM; FEEDING BEHAVIOR; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GOLDFISH; INTERNEURONS; MALE; MEDULLA OBLONGATA; MEMBRANE POTENTIALS; MOTOR NEURONS; NEURAL PATHWAYS; NEUROTRANSMITTER AGENTS; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; REFLEX; SOLITARY NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 69449106380     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22097     Document Type: Article

References (52)

1. Altschuler SM. 2001. Laryngeal and respiratory protective reflexes. Am J Med 111(Suppl 8A):90S-94S.
2. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. 1989. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248-268.
3. Anderson K, Böttger B, Lariviere K, Trudeau V, Finger TE. 2002. GABAergic cells in the goldfish vagal lobe. Chem Senses 27:A110.
4. Andresen MC, Yang MY. 1990. Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am J Physiol 259(Pt 2):H1307-1311.
5. Atema J. 1971. Structures and functions of the sense of taste in the catfish (Ictalurus natalis). Brain Behav Evol 4:273-294.
6. Aylwin ML, Horowitz JM, Bonham AC. 1997. NMDA receptors contribute to primary visceral afferent transmission in the nucleus of the solitary tract. J Neurophysiol 77:2539-2548.
7. Bao H, Bradley RM, Mistretta CM. 1995. Development of intrinsic electrophysiological properties in neurons from the gustatory region of rat nucleus of solitary tract. Brain Res Dev Brain Res 86:143-154.
8. Barrett RT, Bao X, Miselis RR, Altschuler SM. 1994. Brain stem localization of rodent esophageal premotor neurons revealed by transneuronal passage of pseudorabies virus. Gastroenterology 107:728-737.
9. Bieger D. 1991. Neuropharmacologic correlates of deglutition: lessons from fictive swallowing. Dysphagia 6:147-164.
10. Bradley RM, Cheal ML, Kim YH. 1980. Quantitative analysis of developing epiglottal taste buds in sheep. J Anat 130:25-32.
11. Bradley RM, Kim M. 2006. Reflex connections. In: Bradley RM, editor. The role of the solitary tract in gustatory processing. Boca Raton, FL: CRC Press. p 67-82.
12. Bradley RM, King MS, Wang L, Shu X. 1996. Neurotransmitter and neuromodulator activity in the gustatory zone of the nucleus tractus solitarius. Chem Senses 21:377-385.
13. Callan WT, Sanderson SL. 2003. Feeding mechanisms in carp: crossflow filtration, palatal protrusions and flow reversals. J Exp Biol 206:883-892.
14. Cunningham ET Jr, Sawchenko PE. 1989. A circumscribed projection from the nucleus of the solitary tract to the nucleus ambiguus in the rat: anatomical evidence for somatostatin-28-immunoreactive interneurons subserving reflex control of esophageal motility. J Neurosci 9:1668-1682.
15. Cunningham ET Jr, Sawchenko PE. 2000. Dorsal medullary pathways subserving oromotor reflexes in the rat: implications for the central neural control of swallowing. J Comp Neurol 417:448-466.
16. Farrell WJ, Bottger B, Ahmadi F, Finger TE. 2002. Distribution of cholecystokinin, calcitonin gene-related peptide, neuropeptide Y, and galanin in the primary gustatory nuclei of the goldfish. J Comp Neurol 450:103-114.
17. Finger TE. 1988. Sensorimotor mapping and oropharyngeal reflexes in goldfish, Carassius auratus. Brain Behav Evol 31:17-24.
18. Finger TE. 2008. Sorting food from stones: the vagal taste system in goldfish, Carassius auratus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194:135-143.
19. Finger TE, Dunwiddie TV. 1992. Evoked responses from an in vitro slice preparation of a primary gustatory nucleus: the vagal lobe of goldfish. Brain Res 580:27-34.
20. Goehler LE, Finger TE. 1992. Functional organization of vagal reflex systems in the brain stem of the goldfish, Carassius auratus. J Comp Neurol 319:463-478.
21. Hayakawa T, Zheng JQ, Yajima Y. 1997. Direct synaptic projections to esophageal motoneurons in the nucleus ambiguus from the nucleus of the solitary tract of the rat. J Comp Neurol 381:18-30.
22. Hayakawa T, Zheng JQ, Seki M, Yajima Y. 1998. Synaptology of the direct projections from the nucleus of the solitary tract to pharyngeal motoneurons in the nucleus ambiguus of the rat. J Comp Neurol 393:391-401.
23. Hayakawa T, Takanaga A, Maeda S, Ito H, Seki M. 2000. Monosynaptic inputs from the nucleus tractus solitarii to the laryngeal motoneurons in the nucleus ambiguus of the rat. Anat Embryol (Berl) 202:411-420.
24. Huesa G, Ikenaga T, Bottger B, Finger TE. 2008. Calcium-fluxing glutamate receptors associated with primary gustatory afferent terminals in goldfish (Carassius auratus). J Comp Neurol 506:694-707.
25. Ikenaga T, Huesa G, Finger TE. 2006. Co-occurrence of calcium-binding proteins and calcium-permeable glutamate receptors in the primary gustatory nucleus of goldfish. J Comp Neurol 499:90-105.
26. Ikenaga T, Ogura T, Finger TE. 2007. Neurotransmitters in brainstem gustatory reflex circuitry. Chem Senses 32:A44.
27. Jean A. 2001. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 81:929-969.
28. Katz DM, Karten HJ. 1983. Visceral representation within the nucleus of the tractus solitarius in the pigeon, Columba livia. J Comp Neurol 218:42-73.
29. Kessler JP. 1993. Involvement of excitatory amino acids in the activity of swallowing-related neurons of the ventro-lateral medulla. Brain Res 603:353-357.
30. Kim M, Chiego DJ Jr, Bradley RM. 2008. Ionotropic glutamate receptor expression in preganglionic neurons of the rat inferior salivatory nucleus. Auton Neurosci 138:83-90.
31. Kitagawa J, Shingai T, Takahashi Y, Yamada Y. 2002. Pharyngeal branch of the glossopharyngeal nerve plays a major role in reflex swallowing from the pharynx. Am J Physiol Regul Integr Comp Physiol 282:R1342-1347.
32. Kotrschal K, Palzenberger M. 1992. Neuroecology of cyprinids: comparative, quantitative histology reveals diverse brain patterns. Environ Biol Fishes 33:135-152.
33. Lamb CF, Finger TE. 1995. Gustatory control of feeding behavior in goldfish. Physiol Behav 57:483-488.
34. Li CS, Smith DV. 1997. Glutamate receptor antagonists block gustatory afferent input to the nucleus of the solitary tract. J Neurophysiol 77:1514-1525.
35. Lu WY, Bieger D. 1998. Vagal afferent transmission in the NTS mediating reflex responses of the rat esophagus. Am J Physiol 274(Pt 2):R1436-1445.
36. Miller AJ. 2002. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med 13:409-425.
37. Morita Y, Finger TE. 1985. Reflex connections of the facial and vagal gustatory systems in the brainstem of the bullhead catfish, Ictalurus nebulosus. J Comp Neurol 231:547-558.
38. Morita Y, Ito H, Masai H. 1980. Central gustatory paths in the crucian carp, Carassius carassius. J Comp Neurol 191:119-132.
39. Neff RA, Mihalevich M, Mendelowitz D. 1998. Stimulation of NTS activates Research in Systems Neuroscience The Journal of Comparative Neurology NMDA and non-NMDA receptors in rat cardiac vagal neurons in the nucleus ambiguus. Brain Res 792:277-282.
40. Powley TL. 2000. Vagal circuitry mediating cephalic-phase responses to food. Appetite 34:184-188.
41. Sharp AA, Finger TE. 2002. GABAergic modulation of primary gustatory afferent synaptic efficacy. J Neurobiol 52:133-143.
42. Sibbing FA, Uribe R. 1985. Regional specializations in the oropharyngeal wall and food processing in the carp (Cyprinus carpio L.). Neth J Zool 35:377-422.
43. Sibbing FA, Osse JMW, Terlouw A. 1986. Food handling in the carp ( Cyrinus carpio): its movement patterns, mechanisms, and limitations. J Zool 210:161-203.
44. Smeraski CA, Dunwiddie TV, Diao LH, Magnusson KR, Finger TE. 1996. Glutamate receptors mediate synaptic responses in the primary gustatory nucleus in goldfish. Soc Neurosci Abstr 22:1826.
45. Smeraski CA, Dunwiddie TV, Diao L, Finger TE. 1998. Excitatory amino acid neurotransmission in the primary gustatory nucleus of the goldfish Carassius auratus. Ann N Y Acad Sci 855:442-449.
46. Smeraski CA, Dunwiddie TV, Diao L, Finger TE. 1999. NMDA and non-NMDA receptors mediate responses in the primary gustatory nucleus in goldfish. Chem Senses 24:37-46.
47. Smeraski CA, Bottger B, Finger TE. 2001. Kainate-activated cobalt uptake in the primary gustatory nucleus in goldfish: visualization of the morphology and distribution of cells expressing AMPA/kainate receptors in the vagal lobe. J Comp Neurol 431:59-74.
48. Smetters D, Majewska A, Yuste R. 1999. Detecting action potentials in neuronal populations with calcium imaging. Methods 18:215-221.
49. Smith DV, Li CS, Davis BJ. 1998. Excitatory and inhibitory modulation of taste responses in the hamster brainstem. Ann N Y Acad Sci 855:450-456.
50. Wang YT, Bieger D, Neuman RS. 1991a. Activation of NMDA receptors is necessary for fast information transfer at brainstem vagal motoneurons. Brain Res 567:260-266.
51. Wang YT, Neuman RS, Bieger D. 1991b. Somatostatin inhibits nicotinic cholinoceptor mediated-excitation in rat ambigual motoneurons in vitro. Neurosci Lett 123:236-239.
52. Yajima Y, Hayakawa T, Hayashi Y. 1997. Evidence for GABAA receptor-mediated inhibition in ambiguous motoneurons. Acta Otolaryngol Suppl 532:132-134.