Morphology and connectivity of parabrachial and cortical inputs to gustatory thalamus in rats
dc.contributor.author | Holtz, Stephen L. | en_US |
dc.contributor.author | Fu, Anqi | en_US |
dc.contributor.author | Loflin, Wyatt | en_US |
dc.contributor.author | Corson, James A. | en_US |
dc.contributor.author | Erisir, Alev | en_US |
dc.date.accessioned | 2014-12-09T16:54:08Z | |
dc.date.available | 2016-03-02T19:36:56Z | en |
dc.date.issued | 2015-01-01 | en_US |
dc.identifier.citation | Holtz, Stephen L.; Fu, Anqi; Loflin, Wyatt; Corson, James A.; Erisir, Alev (2015). "Morphology and connectivity of parabrachial and cortical inputs to gustatory thalamus in rats." Journal of Comparative Neurology 523(1): 139-161. | en_US |
dc.identifier.issn | 0021-9967 | en_US |
dc.identifier.issn | 1096-9861 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/109654 | |
dc.description.abstract | The ventroposterior medialis parvocellularis (VPMpc) nucleus of the thalamus, the thalamic relay nucleus for gustatory sensation, receives primary input from the parabrachial nucleus, and projects to the insular cortex. To reveal the unique properties of the gustatory thalamus in comparison with archetypical sensory relay nuclei, this study examines the morphology of synaptic circuitry in the VPMpc, focusing on parabrachiothalamic driver input and corticothalamic feedback. Anterogradely visualized parabrachiothalamic fibers in the VPMpc bear large swellings. At electron microscope resolution, parabrachiothalamic axons are myelinated and make large boutons, forming multiple asymmetric, adherent, and perforated synapses onto large‐caliber dendrites and dendrite initial segments. Labeled boutons contain dense‐core vesicles, and they resemble a population of terminals within the VPMpc containing calcitonin gene‐related peptide. As is typical of primary inputs to other thalamic nuclei, parabrachiothalamic terminals are over five times larger than other inputs, while constituting only 2% of all synapses. Glomeruli and triadic arrangements, characteristic features of other sensory thalamic nuclei, are not encountered. As revealed by anterograde tracer injections into the insular cortex, corticothalamic projections in the VPMpc form a dense network of fine fibers bearing small boutons. Corticothalamic terminals within the VPMpc were also observed to synapse on cells that were retrogradely filled from the same injections. The results constitute an initial survey describing unique anatomical properties of the rodent gustatory thalamus. J. Comp. Neurol. 523:139–161, 2015. © 2014 Wiley Periodicals, Inc. Using biotinylated tract tracers and light and electron microscopy, the authors provide quantitative ultrastructural characterization of two inputs that arrive to the gustatory thalamic nucleus (ventroposterior medialis parvocellularis nucleus [VPMpc]): parabrachiothalamic axons that bring the primary input, and corticothalamic axons that provide the feedback input. | en_US |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.publisher | Academic Press | en_US |
dc.subject.other | Rid_000042 | en_US |
dc.subject.other | Nlx_152120 | en_US |
dc.subject.other | Nif‐0000–23420 | en_US |
dc.subject.other | Ventroposteromedial Thalamus | en_US |
dc.subject.other | Cortical Feedback | en_US |
dc.subject.other | CGRP | en_US |
dc.subject.other | Electron Microscopy | en_US |
dc.subject.other | 3D Reconstruction | en_US |
dc.subject.other | RGD_70508 | en_US |
dc.subject.other | AB_2336827 | en_US |
dc.subject.other | AB_259000 | en_US |
dc.subject.other | AB_2336171 | en_US |
dc.title | Morphology and connectivity of parabrachial and cortical inputs to gustatory thalamus in rats | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/109654/1/cne23673.pdf | |
dc.identifier.doi | 10.1002/cne.23673 | en_US |
dc.identifier.source | Journal of Comparative Neurology | en_US |
dc.identifier.citedreference | Samuelsen CLC, Gardner MPHM, Fontanini A. 2013. Thalamic contribution to cortical processing of taste and expectation. J Neurosci 33: 1815 – 1827. | en_US |
dc.identifier.citedreference | Norgren R, Wolf G. 1975. Projections of thalamic gustatory and lingual areas in the rat. Brain Res 92: 123 – 129. | en_US |
dc.identifier.citedreference | Ogawa H, Nomura T. 1988. Receptive field properties of thalamo‐cortical taste relay neurons in the parvicellular part of the posteromedial ventral nucleus in rats. Exp Brain Res 73: 364 – 370. | en_US |
dc.identifier.citedreference | Orazzo C, Pieribone VA, Ceccatelli S, Terenius L, Hökfelt T. 1993. CGRP‐like immunoreactivity in A11 dopamine neurons projecting to the spinal cord and a note on CGRP‐CCK cross‐reactivity. Brain Res 600: 39 – 48. | en_US |
dc.identifier.citedreference | Paxinos G, Watson C. 2007. The rat brain in stereotaxic coordinates. San Diego, CA: Academic Press. | en_US |
dc.identifier.citedreference | Piette CE, Baez‐Santiago MA, Reid EE, Katz DB, Moran A. 2012. Inactivation of basolateral amygdala specifically eliminates palatability‐related information in cortical sensory responses. J Neurosci 32: 9981 – 9991. | en_US |
dc.identifier.citedreference | Poulet JFA, Fernandez LMJ, Crochet S, Petersen CCH. 2012. Thalamic control of cortical states. Nat Neurosci 15: 370 – 372. | en_US |
dc.identifier.citedreference | Pritchard TC, Hamilton RB, Morse JR, Norgren R. 1986. Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J Comp Neurol 244: 213 – 228. | en_US |
dc.identifier.citedreference | Pritchard TC, Hamilton RB, Norgren R. 2000. Projections of the parabrachial nucleus in the Old World monkey. Exp Neurol 165: 101 – 117. | en_US |
dc.identifier.citedreference | Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG. 2000. Pathway tracing using biotinylated dextran amines. J Neurosci Methods 103: 23 – 37. | en_US |
dc.identifier.citedreference | Samuelsen CL, Gardner MPH, Fontanini A. 2012. Effects of cue‐triggered expectation on cortical processing of taste. Neuron 74: 410 – 422. | en_US |
dc.identifier.citedreference | Saul AB. 2008. Lagged cells in alert monkey lateral geniculate nucleus. Vis Neurosci 25: 647 – 659. | en_US |
dc.identifier.citedreference | Scott TR, Erickson RP. 1971. Synaptic processing of taste‐quality information in thalamus of the rat. J Neurophysiol 34: 868 – 883. | en_US |
dc.identifier.citedreference | Scott TR, Yalowitz MS. 1978. Thalamic taste responses to changing stimulus concentration. Chem Senses 3: 167 – 175. | en_US |
dc.identifier.citedreference | Sewards TV. 2004. Dual separate pathways for sensory and hedonic aspects of taste. Brain Res Bull 62: 271 – 283. | en_US |
dc.identifier.citedreference | Sherman SM. 2007. The thalamus is more than just a relay. Curr Opin Neurobiol 17: 417 – 422. | en_US |
dc.identifier.citedreference | Sherman SM, Guillery RW. 2001. Exploring the thalamus. San Diego, CA: Academic Press. | en_US |
dc.identifier.citedreference | Sillito AM, Jones HE. 2002. Corticothalamic interactions in the transfer of visual information. Philos Trans R Soc Lond B Biol Sci 357: 1739 – 1752. | en_US |
dc.identifier.citedreference | Spector AC, Travers SP. 2005. The representation of taste quality in the mammalian nervous system. Behav Cogn Neurosci Rev 4: 143 – 191. | en_US |
dc.identifier.citedreference | Stapleton JR, Lavine ML, Wolpert RL, Nicolelis MAL, Simon SA. 2006. Rapid taste responses in the gustatory cortex during licking. J Neurosci 26: 4126 – 4138. | en_US |
dc.identifier.citedreference | Stehberg J, Acuña‐Goycolea C, Ceric F, Torrealba F. 2001. The visceral sector of the thalamic reticular nucleus in the rat. Neuroscience 106: 745 – 755. | en_US |
dc.identifier.citedreference | Tokita K, Inoue T, Boughter JD Jr. 2010. Subnuclear organization of parabrachial efferents to the thalamus, amygdala and lateral hypothalamus in C57BL/6J mice: a quantitative retrograde double labeling. Neuroscience 171: 351 – 365. | en_US |
dc.identifier.citedreference | Verhagen JV, Giza BK, Scott TR. 2003. Responses to taste stimulation in the ventroposteromedial nucleus of the thalamus in rats. J Neurophysiol 89: 265 – 275. | en_US |
dc.identifier.citedreference | Verhagen JV, Giza BK, Scott TR. 2005. Effect of amiloride on gustatory responses in the ventroposteromedial nucleus of the thalamus in rats. J Neurophysiol 93: 157 – 166. | en_US |
dc.identifier.citedreference | Wang S, Corson JA, Hill DL, Erisir A. 2012. Postnatal development of chorda tympani axons in the rat nucleus of the solitary tract. J Comp Neurol 520: 3217 – 3235. | en_US |
dc.identifier.citedreference | Williamson AM, Ralston HJ. 1993. Fine structure of calcitonin gene‐related peptide immunoreactive synaptic contacts in the thalamus of the rat. J Comp Neurol 328: 130 – 144. | en_US |
dc.identifier.citedreference | Wong HC, Taché Y, Lloyd KC, Yang H, Sternini C, Holzer P, Walsh JH. 2014. Monoclonal antibody to rat alpha‐CGRP: production, characterization, and in vivo immunoneutralization activity. Hybridoma 12: 93 – 106. | en_US |
dc.identifier.citedreference | Yasui Y, Saper CB, Cechetto DF. 1989. Calcitonin gene‐related peptide immunoreactivity in the visceral sensory cortex, thalamus, and related pathways in the rat. J Comp Neurol 290: 487 – 501. | en_US |
dc.identifier.citedreference | Yasui Y, Saper CB, Cechetto DF. 1991. Calcitonin gene‐related peptide (CGRP) immunoreactive projections from the thalamus to the striatum and amygdala in the rat. J Comp Neurol 308: 293 – 310. | en_US |
dc.identifier.citedreference | Zhang L, Hoff AO, Wimalawansa SJ, Cote GJ, Gagel RF, Westlund KN. 2001. Arthritic calcitonin/alpha calcitonin gene‐related peptide knockout mice have reduced nociceptive hypersensitivity. Pain 89: 265 – 273. | en_US |
dc.identifier.citedreference | Zhang Y, Yan J. 2008. Corticothalamic feedback for sound‐specific plasticity of auditory thalamic neurons elicited by tones paired with basal forebrain stimulation. Cereb Cortex 18: 1521 – 1528. | en_US |
dc.identifier.citedreference | Allen GV, Saper CB, Hurley KM, Cechetto DF. 1991. Organization of visceral and limbic connections in the insular cortex of the rat. J Comp Neurol 311: 1 – 16. | en_US |
dc.identifier.citedreference | Bartlett EL, Stark JM, Guillery RW, Smith PH. 2000. Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience 100: 811 – 828. | en_US |
dc.identifier.citedreference | Beckstead RM, Morse JR, Norgren R. 1980. The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei. J Comp Neurol 190: 259 – 282. | en_US |
dc.identifier.citedreference | Benjamin RM, Akert K. 1959. Cortical and thalamic areas involved in taste discrimination in the albino rat. J Comp Neurol 111: 231 – 259. | en_US |
dc.identifier.citedreference | Bester H, Bourgeais L, Villanueva L, Besson JM, Bernard JF. 1999. Differential projections to the intralaminar and gustatory thalamus from the parabrachial area: a PHA‐L study in the rat. J Comp Neurol 405: 421 – 449. | en_US |
dc.identifier.citedreference | Blum M, Walker AE, Ruch TC. 1943. Localization of taste in the thalamus of Macaca mulatta. Yale J Biol Med 16: 175 – 192.1. | en_US |
dc.identifier.citedreference | Briggs F, Usrey WM. 2008. Emerging views of corticothalamic function. Curr Opin Neurobiol 18: 403 – 407. | en_US |
dc.identifier.citedreference | Carleton A, Accolla R, Simon SA. 2010. Coding in the mammalian gustatory system. Trends Neurosci 33: 326 – 334. | en_US |
dc.identifier.citedreference | Cechetto DF, Saper CB. 1987. Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 262: 27 – 45. | en_US |
dc.identifier.citedreference | Coolen LM, Veening JG, Petersen DW, Shipley MT. 2003. Parvocellular subparafascicular thalamic nucleus in the rat: anatomical and functional compartmentalization. J Comp Neurol 463: 117 – 131. | en_US |
dc.identifier.citedreference | Corson JA, Aldridge A, Wilmoth K, Erisir A. 2012. A survey of oral cavity afferents to the rat nucleus tractus solitarii. J Comp Neurol 520: 495 – 527. | en_US |
dc.identifier.citedreference | de Lacalle S, Saper CB. 2000. Calcitonin gene‐related peptide‐like immunoreactivity marks putative visceral sensory pathways in human brain. Neuroscience 100: 115 – 130. | en_US |
dc.identifier.citedreference | Dobolyi A, Irwin S, Makara G, Usdin TB, Palkovits M. 2005. Calcitonin gene‐related peptide‐containing pathways in the rat forebrain. J Comp Neurol 489: 92 – 119. | en_US |
dc.identifier.citedreference | Emmers R. 1964. Localization of thalamic projection of afferents from the tongue in the cat. Anat Rec 148: 67 – 74. | en_US |
dc.identifier.citedreference | Erisir A, Van Horn SC, Sherman SM. 1998. Distribution of synapses in the lateral geniculate nucleus of the cat: differences between laminae A and A1 and between relay cells and interneurons. J Comp Neurol 390: 247 – 255. | en_US |
dc.identifier.citedreference | Fiala JC. 2005. Reconstruct: a free editor for serial section microscopy. J Microsc 218: 52 – 61. | en_US |
dc.identifier.citedreference | Guillery RW, Sherman SM. 2002. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33: 163 – 175. | en_US |
dc.identifier.citedreference | Halsell CB, Travers SP. 1997. Anterior and posterior oral cavity responsive neurons are differentially distributed among parabrachial subnuclei in rat. J Neurophysiol 78: 920 – 938. | en_US |
dc.identifier.citedreference | Hamilton RB, Norgren R. 1984. Central projections of gustatory nerves in the rat. J Comp Neurol 222: 560 – 577. | en_US |
dc.identifier.citedreference | Hanamori T. 2003. Chemical stimulation of the thalamic reticular nucleus inhibits the neuronal activity of the posterior insular cortex in rats. Chem Senses 28: 717 – 728. | en_US |
dc.identifier.citedreference | Hayama T, Hashimoto K, Ogawa H. 1994. Anatomical location of a taste‐related region in the thalamic reticular nucleus in rats. Neurosci Res 18: 291 – 299. | en_US |
dc.identifier.citedreference | Herbert H, Moga MM, Saper CB. 1990. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 293: 540 – 580. | en_US |
dc.identifier.citedreference | Karimnamazi H, Travers JB. 1998. Differential projections from gustatory responsive regions of the parabrachial nucleus to the medulla and forebrain. Brain Res 813: 283 – 302. | en_US |
dc.identifier.citedreference | Katz DB, Simon SA, Nicolelis MA. 2001. Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci 21: 4478 – 4489. | en_US |
dc.identifier.citedreference | Kosar E, Grill HJ, Norgren R. 1986a. Gustatory cortex in the rat. II. Thalamocortical projections. Brain Res 379: 342 – 352. | en_US |
dc.identifier.citedreference | Kosar E, Grill HJ, Norgren R. 1986b. Gustatory cortex in the rat. I. Physiological properties and cytoarchitecture. Brain Res 379: 329 – 341. | en_US |
dc.identifier.citedreference | Kresse A, Jacobowitz DM, Skofitsch G. 1995. Detailed mapping of CGRP mRNA expression in the rat central nervous system: comparison with previous immunocytochemical findings. Brain Res Bull 36: 261 – 274. | en_US |
dc.identifier.citedreference | Krout KE, Loewy AD. 2000. Parabrachial nucleus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 428: 475 – 494. | en_US |
dc.identifier.citedreference | Lasiter PS, Kachele DL. 1988. Postnatal development of the parabrachial gustatory zone in rat: dendritic morphology and mitochondrial enzyme activity. Brain Res Bull 21: 79 – 94. | en_US |
dc.identifier.citedreference | Li L, Ebner FF. 2007. Cortical modulation of spatial and angular tuning maps in the rat thalamus. J Neurosci 27: 167 – 179. | en_US |
dc.identifier.citedreference | Liu XB, Honda CN, Jones EG. 1995. Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352: 69 – 91. | en_US |
dc.identifier.citedreference | Lundy RF, Norgren R. 2004. Gustatory system. In: Paxinos G, editor. The rat nervous system, 3rd ed. San Diego, CA: Academic Press. p 890 – 921. | en_US |
dc.identifier.citedreference | Malpeli JG. 1983. Activity of cells in area 17 of the cat in absence of input from layer a of lateral geniculate nucleus. J Neurophysiol 49: 595 – 610. | en_US |
dc.identifier.citedreference | May OL, Erisir A, Hill DL. 2007. Ultrastructure of primary afferent terminals and synapses in the rat nucleus of the solitary tract: comparison among the greater superficial petrosal, chorda tympani, and glossopharyngeal nerves. J Comp Neurol 502: 1066 – 1078. | en_US |
dc.identifier.citedreference | Nakashima M, Uemura M, Yasui Y, Ozaki HS, Tabata S, Taen A. 2000. An anterograde and retrograde tract‐tracing study on the projections from the thalamic gustatory area in the rat: distribution of neurons projecting to the insular cortex and amygdaloid complex. Neurosci Res 36: 297 – 309. | en_US |
dc.identifier.citedreference | Nomura T, Ogawa H. 1985. The taste and mechanical response properties of neurons in the parvicellular part of the thalamic posteromedial ventral nucleus of the rat. Neurosci Res 3: 91 – 105. | en_US |
dc.identifier.citedreference | Norgren R. 1974. Gustatory afferents to ventral forebrain. Brain Res 81: 285 – 295. | en_US |
dc.identifier.citedreference | Norgren R. 1976. Taste pathways to hypothalamus and amygdala. J Comp Neurol 166: 17 – 30. | en_US |
dc.identifier.citedreference | Norgren R, Leonard CM. 1971. Taste pathways in rat brainstem. Science 173: 1136 – 1139. | en_US |
dc.identifier.citedreference | Norgren R, Leonard CM. 1973. Ascending central gustatory pathways. J Comp Neurol 150: 217 – 237. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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