Substance P containing and cholinergic projections from the habenula
Abstract
Electrolytic lesions and surgical transection of the habenulo-interpeduncular-ventrotegmental tract have established the existence of separate habenulo-interpeduncular-ventrotegmental substance P and cholinergic projections. Micro-knife lesions separating the habenula nuclei showed the medial habenular nucleus to be the source of substance P fibres running via the fasciculus retroflexus to the ventral tegmental area. The lateral habenular nucleus receives a substance P projection from the medial habenular nucleus and is the source of cholinergic projection to the interpeduncular nucleus and to the medial habenular nucleus. Lesions of the ventrotegmental-interpeduncular area did not modify the levels of substance P and choline acetyltransferase in the habenula. These observations suggested that there are no substance P or ACh containing afferents to the habenula from the ventrotegmental-interpeduncular area and the accumulation of substance P and AChE proximal to but not caudal to transections of the fasciculus retroflexus confirmed this view.
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The MHb contains neurons that produce acetylcholine or substance P, and a small population that produces interleukin-18.
“MHb is comprised of neurons that produce the neurotransmitters acetylcholine (ACh) or substance P (Cuello et al. 1978;Eckenrode et al. 1987), and a small population that produce the cytokine interleukin-18 (IL-18) (Sugama et al. 2002).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Cuello et al. 1978
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,143 · see citing works
LOCALIZATION OF ANTIGEN IN TISSUE CELLS
Coons, A. H., & Kaplan, M. H. (1950) · The Journal of Experimental Medicine · doi:10.1084/jem.91.1.1 · Cited by 1,906 · see citing works
An unidentified depressor substance in certain tissue extracts
von Euler, U. S., & Gaddum, J. H. (1931) · The Journal of Physiology · doi:10.1113/jphysiol.1931.sp002763 · Cited by 1,584 · see citing works
A Histochemical Method for Localizing Cholinesterase Activity.
Koelle, G. B., & Friedenwald, J. S. (1949) · Experimental Biology and Medicine · doi:10.3181/00379727-70-17013 · Cited by 1,192 · see citing works
Fonnum, F. (1969) · Biochemical Journal · doi:10.1042/bj1150465 · Cited by 1,037 · see citing works
Substance P: Localization in the Central Nervous System and in Some Primary Sensory Neurons
Hökfelt, T. G. M., Kellerth, J. ‐., Nilsson, G., & Pernow, B. (1975) · Science · doi:10.1126/science.242075 · Cited by 1,024 · see citing works
Herkenham, M. A., & Nauta, W. J. H. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901730107 · Cited by 798 · see citing works
Amino-acid Sequence of Substance P
CHANG, M. M., Leeman, S. E., & Niall, H. D. (1971) · Nature New Biology · doi:10.1038/newbio232086a0 · Cited by 790 · see citing works
The distribution of substance P immunoreactive fibers in the rat central nervous system
Cuello, A. C., & Kanazawa, I. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901780108 · Cited by 728 · see citing works
Chang, M. M., & Leeman, S. E. (1970) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)62860-1 · Cited by 699 · see citing works
Do some nerve cells release more than one transmitter?
Burnstock, G. (1976) · Neuroscience · doi:10.1016/0306-4522(76)90054-3 · Cited by 640 · see citing works
Mesencephalic dopamine neurons projecting to neocortex
Lindvall, O., Björklund, A., Moore, R. Y., & Stenevi, U. (1974) · Brain Research · doi:10.1016/0006-8993(74)90947-0 · Cited by 504 · see citing works
Regional distribution of substance P in the brain of the rat
Brownstein, M., Mroz, E. A., Kizer, J. S., Palkovits, M., & Leeman, S. E. (1976) · Brain Research · doi:10.1016/0006-8993(76)90907-0 · Cited by 417 · see citing works
Post morten changes and regional distribution of substance P in the rat and mouse nervous system
Kanazawa, I., & Jessell, T. M. (1976) · Brain Research · doi:10.1016/0006-8993(76)90748-4 · Cited by 311 · see citing works
Self-citationUltrastructural localization of substance P in neurons of spinal cord
Pickel, V. M., Reis, D. J., & Leeman, S. E. (1977) · Brain Research · doi:10.1016/0006-8993(77)90463-2 · Cited by 301 · see citing works
The origin and distribution of dopamine-containing afferents to the rat frontal cortex
Emson, P. C., & Koob, G. F. (1978) · Brain Research · doi:10.1016/0006-8993(78)90634-0 · Cited by 287 · see citing works
Self-citationRelease of substance P-like immunoreactivity from isolated spinal cord of newborn rat
Otsuka, M., & Konishi, S. (1976) · Nature · doi:10.1038/264083a0 · Cited by 287 · see citing works
Substance P and Excitatory Transmitter of Primary Sensory NeuronsPreprint
Otsuka, M., & Konishi, S. (1976) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1976.040.01.015 · Cited by 244 · see citing works
Radioimmunoassay for Substance P
POWELL, D., Leeman, S. E., Tregear, G. W., Niall, H. D., & Potts, J. T. J. (1973) · Nature New Biology · doi:10.1038/newbio241252a0 · Cited by 226 · see citing works
Coexistence of Several Putative Neurotransmitters in Single Identified Neurosn of Aplysia
Brownstein, M., Saavedra, J. M., Axelrod, J., Zeman, G. H., & Carpenter, D. O. (1974) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.71.12.4662 · Cited by 179 · see citing works
Hyperphagia produced by knife cuts between the medial and lateral hypothalamus in the rat
Sclafani, A. J., & Grossman, S. P. (1969) · Physiology & Behavior · doi:10.1016/0031-9384(69)90150-4 · Cited by 167 · see citing works
Habenulo-interpeduncular tract: a possible cholinergic neuron in rat brain
Kataoka, K., Nakamura, Y., & Hassler, R. (1973) · Brain Research · doi:10.1016/0006-8993(73)90639-2 · Cited by 160 · see citing works
Leeman, S. E., & Mroz, E. A. (1974) · Life Sciences · doi:10.1016/0024-3205(74)90020-4 · Cited by 139 · see citing works
SUBSTANCE P: A NATURALLY OCCURRING TRANSMITTER IN HUMAN SPINAL CORD
Cuello, A. C., Polak, J. M., & Pearse, A. G. E. (1976) · The Lancet · doi:10.1016/s0140-6736(76)90968-5 · Cited by 136 · see citing works
Release and metabolism of substance P in rat hypothalamus
Iversen, L. L., Jessell, T. M., & Kanazawa, I. (1976) · Nature · doi:10.1038/264081a0 · Cited by 136 · see citing works
Self-citationSubstance P: localization in synaptic vesicles in rat central nervous system
Cuello, A. C., Jessell, T. M., Kanazawa, I., & Iversen, L. L. (1977) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1977.tb07795.x · Cited by 134 · see citing works
Self-citationIdentified amine-containing neurones and their synaptic connexions
Cottrell, G. A. (1977) · Neuroscience · doi:10.1016/0306-4522(77)90064-1 · Cited by 129 · see citing works
The connections of the habenula in the rabbit
Cragg, B. G. (1961) · Experimental Neurology · doi:10.1016/0014-4886(61)90013-9 · Cited by 123 · see citing works
Evidence for substance P in the habenulo-interpeduncular tract
Mroz, E. A., Brownstein, M., & Leeman, S. E. (1976) · Brain Research · doi:10.1016/0006-8993(76)90061-5 · Cited by 113 · see citing works
Nilsson, G., Hökfelt, T. G. M., & Pernow, B. (1974) · PubMed · Cited by 111 · see citing works
Release of substance P from isolated nerve endings
SCHENKER, C., Mroz, E. A., & Leeman, S. E. (1976) · Nature · doi:10.1038/264790a0 · Cited by 103 · see citing works
Effects of habenular lesions on the substance P content of various brain regions
Hong, J., Costa, E., & Yang, H. (1976) · Brain Research · doi:10.1016/0006-8993(76)90325-5 · Cited by 91 · see citing works
Substance P release from the rat substantia nigra
Jessell, T. M. (1978) · Brain Research · doi:10.1016/0006-8993(78)91080-6 · Cited by 90 · see citing works
Self-citationSmaha, L. A., & Kaelber, W. W. (1973) · Experimental Brain Research · doi:10.1007/bf00233332 · Cited by 76 · see citing works
Leranth, C., Brownstein, M. J., Záborszky, L., Járányi, Z., & Palkovits, M. (1975) · Brain Research · doi:10.1016/0006-8993(75)90613-7 · Cited by 64 · see citing works
Connections of the habenula and of the interpeduncular nucleus in the cat
Mitchell, R. A. (1963) · The Journal of Comparative Neurology · doi:10.1002/cne.901210311 · Cited by 58 · see citing works
Distribution and release of Substance P in the central nervous system
Cuello, A. C., Emson, P. C., Fiacco, M. D., Gale, J. S., Iversen, L. L., Jessell, T. M., Kanazawa, I., Paxinos, G., & Quik, M. (1978) · Palgrave Macmillan UK eBooks · doi:10.1007/978-1-349-03668-4_9 · Cited by 55 · see citing works
Self-citationKoob, G. F., Balcom, G. J., & Meyerhoff, J. L. (1975) · Brain Research · doi:10.1016/0006-8993(75)90875-6 · Cited by 54 · see citing works
A new interpedunculo‐diencephalic pathway in rats and cats
Massopust, L. C., & Thompson, R. (1962) · The Journal of Comparative Neurology · doi:10.1002/cne.901180108 · Cited by 45 · see citing works
Substance-P Pathways in Rat Brain
Emson, P. C., Kanazawa, I., Cuello, A. C., & Jessell, T. M. (1977) · Biochemical Society Transactions · doi:10.1042/bst0050187 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity
Oades, R. D., & Halliday, G. M. (1987) · Brain Research Reviews · doi:10.1016/0165-0173(87)90011-7 · Cited by 1,001 · see citing works
Efferent connections of the habenular nuclei in the rat
Herkenham, M. A., & Nauta, W. J. H. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870103 · Cited by 855 · see citing works
The organization and some projections of cholinergic neurons of the mammalian forebrain
Fibiger, H. C. (1982) · Brain Research Reviews · doi:10.1016/0165-0173(82)90011-x · Cited by 818 · see citing works
Houser, C. R., Crawford, G. D., Barber, R. P., Salvaterra, P. M., & Vaughn, J. E. (1983) · Brain Research · doi:10.1016/0006-8993(83)91312-4 · Cited by 748 · see citing works
Sutherland, R. J. (1982) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(82)90003-3 · Cited by 537 · see citing works
Substance P as a Transmitter Candidate
Nicoll, R. A., SCHENKER, C., & Leeman, S. E. (1980) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.03.030180.001303 · Cited by 528 · see citing works
Circuits and functions of the lateral habenula in health and in disease
Hu, H., Cui, Y., & Yang, Y. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0292-4 · Cited by 471 · see citing works
Christoph, G., Leonzio, R., & Wilcox, K. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-03-00613.1986 · Cited by 418 · see citing works
Simon, H., Moal, M. L., & Calas, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90085-4 · Cited by 401 · see citing works
Ji, H., & Shepard, P. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0958-07.2007 · Cited by 388 · see citing works
Substance P in the Nervous System
Jessell, T. M. (1983) · Springer eBooks · doi:10.1007/978-1-4613-3515-3_1 · Cited by 371 · see citing works
Self-citationCholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase
Wainer, B. H., Levey, A. I., Mufson, E. J., & Mesulam, M. M. (1984) · Neurochemistry International · doi:10.1016/0197-0186(84)90089-5 · Cited by 287 · see citing works
Lecourtier, L., & Kelly, P. H. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.004 · Cited by 283 · see citing works
Diversity of native nicotinic receptor subtypes in mammalian brain
Zoli, M., Pistillo, F., & Gotti, C. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.003 · Cited by 277 · see citing works
Rotter, A., Birdsall, N. J. M., Field, P. M., & Raisman, G. (1979) · Brain Research Reviews · doi:10.1016/0165-0173(79)90003-1 · Cited by 227 · see citing works
McLaughlin, I., Dani, J. A., & Biasi, M. D. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14008 · Cited by 223 · see citing works
Peptides as neurotransmitter candidates in the mammalian cns
Emson, P. C. (1979) · Progress in Neurobiology · doi:10.1016/0301-0082(79)90015-7 · Cited by 209 · see citing works
Self-citationKalivas, P. W., Burgess, S. K., Nemeroff, C. B., & Prange, A. J. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90195-1 · Cited by 208 · see citing works
The cholinergic systems in brain and spinal cord
Kása, P. (1986) · Progress in Neurobiology · doi:10.1016/0301-0082(86)90016-x · Cited by 208 · see citing works
Groenewegen, H. J., Ahlenius, S., Haber, S. N., Kowall, N. W., & Nauta, W. J. H. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490107 · Cited by 202 · see citing works
Genetic dissection of medial habenula–interpeduncular nucleus pathway function in mice
Kobayashi, Y., Sano, Y., Vannoni, E., Goto, H., Suzuki, H., Oba, A., Kawasaki, H., Kanba, S., Lipp, H., Murphy, N. P., et al. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00017 · Cited by 189 · see citing works
Acetylcholinesterase and the cholinergic neuron
Lehmann, J. C., & Fibiger, H. C. (1979) · Life Sciences · doi:10.1016/0024-3205(79)90596-4 · Cited by 187 · see citing works
Gamse, J. T., Kuan, Y., Macurak, M., Brösamle, C., Thisse, B., Thisse, C., & Halpern, M. E. (2005) · Development · doi:10.1242/dev.02046 · Cited by 186 · see citing works
Molecular Mechanisms Underlying Behaviors Related to Nicotine AddictionPreprint
Picciotto, M. R., & Kenny, P. J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012112 · Cited by 178 · see citing works
Extrinsic Sources of Cholinergic Innervation of the Striatal Complex: A Whole-Brain Mapping Analysis
Dautan, D., Bay, H. H., Bolam, J. P., Gerdjikov, T. V., & Mena‐Segovia, J. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00001 · Cited by 172 · see citing works
Transcriptional and spatial resolution of cell types in the mammalian habenula
Hashikawa, Y., Hashikawa, K., Rossi, M. A., Basiri, M. L., Liu, Y., Johnston, N. L., Ahmad, O. R., & Stuber, G. D. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.011 · Cited by 167 · see citing works
Araki, M., McGeer, P. L., & Kimura, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)91410-2 · Cited by 163 · see citing works
Smith, Y., Parent, A., Goff, L. K., & Pelletier, G. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902360107 · Cited by 160 · see citing works
Mechanisms of Nicotine Addiction
Picciotto, M. R., & Kenny, P. J. (2021) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039610 · Cited by 157 · see citing works
Contestabile, R. A., & Flumerfelt, B. A. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901960206 · Cited by 156 · see citing works
The role of the habenula in drug addiction
Velasquez, K. M., Molfese, D. L., & Salas, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00174 · Cited by 155 · see citing works
Habenular and interpeduncularis nuclei: shared components in multiple-function networks.
Klemm, W. R. (2004) · PubMed · Cited by 153 · see citing works
Zhao, H., Zhang, B., Yang, S., & Rusak, B. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.016 · Cited by 147 · see citing works
Interactions between neuropeptides and dopamine neurons in the ventromedial mesencephalon
Kalivas, P. W. (1985) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(85)90004-1 · Cited by 145 · see citing works
Marksteiner, J., Sperk, G., & Krause, J. E. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903170403 · Cited by 142 · see citing works
Contestabile, A., Villani, L., Fasolo, A., Franzoni, M. F., Gribaudo, L., Øktedalen, O., & Fonnum, F. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90337-x · Cited by 136 · see citing works
The medial habenula: still neglected
Viswanath, H., Carter, A. Q., Baldwin, P. R., Molfese, D. L., & Salas, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00931 · Cited by 133 · see citing works
Neurochemical phenotypes of the afferent and efferent projections of the mouse medial habenula
Qin, C., & Luo, M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.085 · Cited by 133 · see citing works
Lisoprawski, A., Herve, D., Blanc, G., Glowinski, J., & Tassin, J. P. (1980) · Brain Research · doi:10.1016/0006-8993(80)90135-3 · Cited by 130 · see citing works
Cholinergic systems in the rat brain: II. Projections to the interpeduncular nucleus
Woolf, N. J., & Butcher, L. L. (1985) · Brain Research Bulletin · doi:10.1016/0361-9230(85)90178-9 · Cited by 130 · see citing works
Parker, M. O., Brock, A. J., Walton, R. T., & Brennan, C. H. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00063 · Cited by 130 · see citing works
Zhang, L., Hernández, V. S., Swinny, J. D., Verma, A. K., Giesecke, T., Emery, A. C., Mutig, K., García‐Segura, L. M., & Eiden, L. E. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0099-5 · Cited by 121 · see citing works
Consciousness and epilepsy: why are complex-partial seizures complex?
Englot, D. J., & Blumenfeld, H. (2009) · Progress in brain research · doi:10.1016/s0079-6123(09)17711-7 · Cited by 119 · see citing works
Pistillo, F., Clementi, F., Zoli, M., & Gotti, C. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.10.002 · Cited by 113 · see citing works
Nicot, A. B., Rostène, W. H., & Bérod, A. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410310 · Cited by 111 · see citing works
Harlan, R. E., Garcia, M. M., & Krause, J. E. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902870204 · Cited by 110 · see citing works
Szigethy, E., & Beaudet, A. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902790111 · Cited by 110 · see citing works
Interpeducular nucleus afferents in the rat
Marchand, E. R., Riley, J. N., & Moore, R. Y. (1980) · Brain Research · doi:10.1016/0006-8993(80)90169-9 · Cited by 109 · see citing works
Anti-addictive actions of an iboga alkaloid congener: a novel mechanism for a novel treatment
Maisonneuve, I. M., & Glick, S. D. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00119-9 · Cited by 108 · see citing works
Arnt, J., & Scheel‐Krüger, J. (1979) · Life Sciences · doi:10.1016/0024-3205(79)90402-8 · Cited by 106 · see citing works
Smith, Y., Séguéla, P., & Parent, A. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90355-1 · Cited by 106 · see citing works
Contestabile, A., & Fonnum, F. (1983) · Brain Research · doi:10.1016/0006-8993(83)90989-7 · Cited by 101 · see citing works
Kelley, A. E., Stinus, L., & Iversen, S. D. (1979) · Neuroscience Letters · doi:10.1016/0304-3940(79)90018-1 · Cited by 98 · see citing works
Hamill, G. S., Olschowka, J. A., Lenn, N. J., & Jacobowitz, D. M. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902260410 · Cited by 94 · see citing works
Clarke, P. B. S., Hamill, G. S., Nadi, N. S., Jacobowitz, D. M., & Pert, A. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902510311 · Cited by 94 · see citing works
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 91 · see citing works
Cholinergic left-right asymmetry in the habenulo-interpeduncular pathway
Hong, E., Santhakumar, K., Akitake, C. A., Ahn, S. J., Thisse, C., Thisse, B., Wyart, C., Mangin, J., & Halpern, M. E. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319566110 · Cited by 82 · see citing works
Valjakka, A., Vartiainen, J., Tuomisto, L. M., Tuomisto, J. T., Olkkonen, H., & Airaksinen, M. M. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00006-9 · Cited by 86 · see citing works
Weld, M. M., & Maler, L. (1992) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(92)90038-r · Cited by 84 · see citing works
Chemical transmission in the rat interpeduncular nucleus in vitro.
Brown, D. A., Docherty, R. J., & Halliwell, J. V. (1983) · The Journal of Physiology · doi:10.1113/jphysiol.1983.sp014831 · Cited by 84 · see citing works
Reiner, A. J., Krause, J. E., Keyser, K. T., Eldred, W. D., & McKelvy, J. F. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902260105 · Cited by 83 · see citing works
Murray, M., Zimmer, J., & Raisman, G. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870211 · Cited by 78 · see citing works
Substance P afferents from the habenula innervate the dorsal raphe nucleus
Neckers, L., Schwartz, J. P., Wyatt, R. J., & Speciale, S. G. (1979) · Experimental Brain Research · doi:10.1007/bf00236830 · Cited by 77 · see citing works
Eison, A. S., Eison, M. S., & Iversen, S. D. (1982) · Brain Research · doi:10.1016/0006-8993(82)90777-6 · Cited by 77 · see citing works
Morley, B. J. (1986) · International review of neurobiology · doi:10.1016/s0074-7742(08)60108-7 · Cited by 76 · see citing works
Hamill, G. S., & Lenn, N. J. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902220307 · Cited by 76 · see citing works
Understanding the habenula: A major node in circuits regulating emotion and motivation
Ables, J. L., Park, K., & Ibáñez-Tallon, I. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106734 · Cited by 76 · see citing works
Transmitters contained in the efferents of the habenula
Vincent, S. R., Staines, W. A., McGeer, E. G., & Fibiger, H. C. (1980) · Brain Research · doi:10.1016/0006-8993(80)90084-0 · Cited by 74 · see citing works
Relevance of the Habenular Complex to Neuropsychiatry: A Review and Hypothesis
Sandyk, R. (1991) · International Journal of Neuroscience · doi:10.3109/00207459108990738 · Cited by 70 · see citing works
Interpeduncular nucleus organization in the rat: Cytoarchitecture and histochemical analysis
Hemmendinger, L. M., & Moore, R. Y. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90018-2 · Cited by 70 · see citing works
A study of afferent projections to the rat interpeduncular nucleus
Hamill, G. S., & Jacobowitz, D. M. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90035-2 · Cited by 68 · see citing works
Neurotransmitter map of the asymmetric dorsal habenular nuclei of zebrafish
deCarvalho, T., Subedi, A., Rock, J. R., Harfe, B. D., Thisse, C., Thisse, B., Halpern, M. E., & Hong, E. (2014) · genesis · doi:10.1002/dvg.22785 · Cited by 67 · see citing works
The Role of the Habenula in Nicotine Addiction
Baldwin, P. R., Alanis, R., & Salas, R. (2012) · Journal of Addiction Research & Therapy · doi:10.4172/2155-6105.s1-002 · Cited by 67 · see citing works
Activation by stress of the habenulo-interpeduncular substance P neurons in the rat
Lisoprawski, A., Blanc, G., & Glowinski, J. (1981) · Neuroscience Letters · doi:10.1016/0304-3940(81)90099-9 · Cited by 67 · see citing works
Basal ganglia organization in amphibians: Chemoarchitecture
Marín, Ó., Smeets, W. J. A. J., & González, A. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980316)392:3 · Cited by 145 · see citing works
Eckenrode, T. C., Barr, G. A., Battisti, W. P., & Murray, M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90095-3 · Cited by 64 · see citing works
Naloxone-reversible analgesia induced by electrical stimulation of the habenula in the rat
Mahieux, G., & Benabid, A. (1987) · Brain Research · doi:10.1016/0006-8993(87)90776-1 · Cited by 64 · see citing works
Nemeroff, C. B., Kalivas, P. W., Golden, R. N., & Prange, A. J. (1984) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(84)90027-5 · Cited by 64 · see citing works
Addiction‐related neuroadaptations following chronic nicotine exposure
Wills, L., & Kenny, P. J. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15356 · Cited by 61 · see citing works
Distribution of tachykinin- and enkephalin-immunoreactive fibers in the human thalamus
Hirai, T., & Jones, E. G. (1989) · Brain Research Reviews · doi:10.1016/0165-0173(89)90008-8 · Cited by 57 · see citing works
Conserved expression of the GPR151 receptor in habenular axonal projections of vertebrates
Jester-Broms, J., Antolin‐Fontes, B., Tingström, A., & Ibáñez-Tallon, I. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23664 · Cited by 54 · see citing works
Sperlágh, B., Maglóczky, Z., Vizi, E. S., & Freund, T. F. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00026-8 · Cited by 54 · see citing works
Maness, L. M., Banks, W. A., Zadina, J. E., & Kastin, A. J. (1995) · Brain Research · doi:10.1016/0006-8993(95)00913-b · Cited by 50 · see citing works
Distribution of Substance P- and Enkephalin-Immunoreactive Neurons and Fibers
Pioro, E. P., MAI, J. K., & Cuello, A. C. (1990) · Elsevier eBooks · doi:10.1016/b978-0-12-547625-6.50037-4 · Cited by 50 · see citing works
Distribution of certain neuropeptides in the primate thalamus
Molinari, M., Hendry, S. H. C., & Jones, E. G. (1987) · Brain Research · doi:10.1016/0006-8993(87)90881-x · Cited by 49 · see citing works
The lateral habenula: A hub for value-guided behavior
Groos, D., & Helmchen, F. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113968 · Cited by 43 · see citing works
Neuroanatomical identification of the frog habenular connections using peroxidase (HRP)
Kemali, M., Guglielmotti, V., & Gioffr�, D. (1980) · Experimental Brain Research · doi:10.1007/bf00236654 · Cited by 47 · see citing works
Origin and distribution of noradrenergic innervation in the habenula: A neurochemical study
Gottesfeld, Z. (1983) · Brain Research · doi:10.1016/0006-8993(83)90990-3 · Cited by 46 · see citing works
Substance P Mechanism in Cluster Headache: Evaluation in Plasma and Cerebrospinal Fluid
Sicuteri, F., Fanciullacci, M., Geppetti, P., Renzi, D., Caleri, D., & Spillantini, M. G. (1985) · Cephalalgia · doi:10.1046/j.1468-2982.1985.0503143.x · Cited by 44 · see citing works
Rønnekleiv, O. K., & Kelly, M. J. (1984) · Journal of Pineal Research · doi:10.1111/j.1600-079x.1984.tb00226.x · Cited by 44 · see citing works
Prominent Narp expression in projection pathways and terminal fields
Reti, I. M., Reddy, R., Worley, P. F., & Baraban, J. M. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01051.x · Cited by 42 · see citing works
Wolters, J. G., ten Donkelaar, H. J., & Verhofstad, A. A. J. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90109-0 · Cited by 42 · see citing works
Medial habenula cholinergic signaling regulates cocaine‐associated relapse‐like behavior
López, A. J., Jia, Y., White, A. O., Kwapis, J. L., Espinoza, M. E., Hwang, P. H., Campbell, R. R., Alaghband, Y., Chitnis, O., Matheos, D. P., et al. (2018) · Addiction Biology · doi:10.1111/adb.12605 · Cited by 40 · see citing works
Rodríguez‐Moldes, I., Manso, M. J., Becerra, M., Molíst, P., & Anadón, R. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903350207 · Cited by 40 · see citing works
Autoradiographic labeling of the cholinergic habenulo-interpeduncular projection
Villani, L., Contestabile, A., & Fonnum, F. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90272-0 · Cited by 40 · see citing works
Localization of Substance P in Neuronal Pathways
Cuello, A. C., Priestley, J. V., & Matthews, M. R. (1982) · Novartis Foundation symposium · doi:10.1002/9780470720738.ch5 · Cited by 40 · see citing works
Cholinergic and non-cholinergic forebrain projections to the interpenduncular nucleus
Albanese, A., Castagna, M., & Altavista, M. C. (1985) · Brain Research · doi:10.1016/0006-8993(85)90545-1 · Cited by 38 · see citing works
Acetylcholine release in interpeduncular nucleus following the stimulation of habenula
Sastry, B. R., Zialkowski, S. E., Hansen, L. M., Kavanagh, J. P., & Evoy, E. M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90032-5 · Cited by 38 · see citing works
Substance P and Its Effects on Learning and Memory
Huston, J. P., & Staubli, U. V. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-474980-1.50030-1 · Cited by 38 · see citing works
Substance P receptor antagonist in lateral habenula improves rat depression-like behavior
Yang, L.-M., Yu, L., Jin, H., & Zhao, H. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.10.007 · Cited by 36 · see citing works
- Authors
- Claudio Cuello, A., Emson, P. C., Paxinos, G., & Jessell, T.
- Affiliations
- University of Cambridge (GB)
- ORCID
- Paxinos, George
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1978-06
- Volume
- 149
- Issue
- 2
- Pages
- 413-429
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2020107272
- Cited by
- 197
- References
- 41
- Citations by year
- 2025: 1 · 2024: 3 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 5 · 2018: 6 · 2017: 4 · 2016: 2 · 2015: 3 · 2014: 9 · 2013: 5 · 2012: 3
- FWCI
- 4.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- substance P, cholinergic projections, habenula, fasciculus retroflexus, ventral tegmental area, interpeduncular nucleus, choline acetyltransferase, afferent projections
- MeSH terms
- Acetylcholinesterase, Animals, Cholinergic Fibers, Fluorescent Antibody Technique, Male, Neural Pathways, Substance P, Tegmentum Mesencephali, Thalamic Nuclei, Rats
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