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Neurochemistry of the Anterior Thalamic Nuclei

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Abstract

This paper reviews the distribution of several bioactive substances and their possible physiological roles in the anterior thalamic nuclei of various species, with a special emphasis on the rat. The anterior thalamus is a part of extended hippocampal system and its significance for learning and memory processes is well known. Although our knowledge about a specific role of this brain structure has increased in recent years considerably, this is the first attempt to summarize neurochemical diversity of the anterior thalamus. The following groups of bioactive substances are reviewed: (1) classical neurotransmitters (gamma-aminobutyric acid, glutamate and aspartate, acetylcholine, serotonin) and their receptors, (2) calcium-binding proteins (calretinin, calbindin, parvalbumin), and (3) others (cocaine- and amphetamine regulated transcript, enkephalins, substance P). In order to extend our knowledge concerning exact functions of selected neurotransmitters and neuromodulators in the studied brain structure, the future studies should concentrate on potential alterations in the neurochemical profile during various pathological states which affect the anterior thalamic nuclei.

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References

  1. Aggleton JP, Brown MW (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22:425–444

    CAS  PubMed  Google Scholar 

  2. Jankowski MM, Ronnqvist KC, Tsanov M, Vann SD, Wright NF, Erichsen JT, Aggleton JP, O’Mara SM (2013) The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front Syst Neurosci 7:45

    Article  PubMed  PubMed Central  Google Scholar 

  3. Aggleton JP, O’Mara SM, Vann SD, Wright NF, Tsanov M, Erichsen JT (2010) Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31:2292–2307

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ghika-Schmid F, Bogousslavsky J (2000) The acute behavioral syndrome of anterior thalamic infarction: a prospective study of 12 cases. Ann Neurol 48:220–227

    Article  CAS  PubMed  Google Scholar 

  5. Harding A, Halliday G, Caine D, Kril J (2000) Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123:141–154

    Article  PubMed  Google Scholar 

  6. Van der Werf YD, Jolles J, Witter MP, Uylings HB (2003) Contributions of thalamic nuclei to declarative memory functioning. Cortex 39:1047–1062

    Article  PubMed  Google Scholar 

  7. Gold JJ, Squire LR (2006) The anatomy of amnesia: neurohistological analysis of three new cases. Learn Mem 13:699–710

    Article  PubMed  PubMed Central  Google Scholar 

  8. Aggleton JP, Neave N, Nagle S, Hunt PR (1995) A comparison of the effects of anterior thalamic, mamillary body and fornix lesions on reinforced spatial alternation. Behav Brain Res 68:91–101

    Article  CAS  PubMed  Google Scholar 

  9. Sziklas V, Petrides M (1999) The effects of lesions to the anterior thalamic nuclei on object-place associations in rats. Eur J Neurosci 11:559–566

    Article  CAS  PubMed  Google Scholar 

  10. Vann SD, Aggleton JP (2003) Evidence of a spatial encoding deficit in rats with lesions of the mammillary bodies or mammillothalamic tract. J Neurosci 23:3506–3514

    CAS  PubMed  Google Scholar 

  11. Mitchell AS, Dalrymple-Alford JC (2006) Lateral and anterior thalamic lesions impair independent memory systems. Learn Mem 13:388–396

    Article  PubMed  PubMed Central  Google Scholar 

  12. Moreau PH, Tsenkina Y, Lecourtier L, Lopez J, Cosquer B, Wolff M, Dalrymple-Alford J, Cassel JC (2013) Lesions of the anterior thalamic nuclei and intralaminar thalamic nuclei: place and visual discrimination learning in the water maze. Brain Struct Funct 218:657–667

    Article  PubMed  Google Scholar 

  13. Aggleton JP, Nelson AJ (2015) Why do lesions in the rodent anterior thalamic nuclei cause such severe spatial deficits? Neurosci Biobehav Rev 54:131–144

    Article  PubMed  PubMed Central  Google Scholar 

  14. Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200:341–354

    Article  CAS  PubMed  Google Scholar 

  15. Yen CT, Conley M, Hendry SH, Jones EG (1985) The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat. J Neurosci 5:2254–2268

    CAS  PubMed  Google Scholar 

  16. Bowery NG, Hudson AL, Price GW (1987) GABAA and GABAB receptor site distribution in the rat central nervous system. Neuroscience 20:365–383

    Article  CAS  PubMed  Google Scholar 

  17. Gonzalo-Ruiz A, Lieberman AR (1995) GABAergic projections from the thalamic reticular nucleus to the anteroventral and anterodorsal thalamic nuclei of the rat. J Chem Neuroanat 9:165–174

    Article  CAS  PubMed  Google Scholar 

  18. Wang B, Gonzalo-Ruiz A, Sanz JM, Campbell G, Lieberman AR (1999) Immunoelectron microscopic study of gamma-aminobutyric acid inputs to identified thalamocortical projection neurons in the anterior thalamus of the rat. Exp Brain Res 126:369–382

    Article  CAS  PubMed  Google Scholar 

  19. Albo Z, Viana Di Prisco G, Vertes RP (2003) Anterior thalamic unit discharge profiles and coherence with hippocampal theta rhythm. Thalamus Relat Syst 2:133–144

    Article  Google Scholar 

  20. Vertes RP, Albo Z, Viana Di Prisco G (2001) Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit. Neuroscience 104:619–625

    Article  CAS  PubMed  Google Scholar 

  21. Vertes RP, Hoover WB, Viana Di Prisco G (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3:173–200

    Article  PubMed  Google Scholar 

  22. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641

    Article  CAS  PubMed  Google Scholar 

  23. Buzsáki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15:827–840

    Article  PubMed  Google Scholar 

  24. Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86

    CAS  PubMed  Google Scholar 

  25. Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207

    Article  CAS  PubMed  Google Scholar 

  26. Tsanov M, Chah E, Vann SD, Reilly RB, Erichsen JT, Aggleton JP, O’Mara SM (2011) Theta-modulated head direction cells in the rat anterior thalamus. J Neurosci 31:9489–9502

    Article  CAS  PubMed  Google Scholar 

  27. Benson DL, Isackson PJ, Gall CM, Jones EG (1992) Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+/calmodulin protein kinase gene expression in the rat central nervous system. Neuroscience 46:825–849

    Article  CAS  PubMed  Google Scholar 

  28. Gonzalo-Ruiz A, Sanz JM, Lieberman AR (1996) Immunohistochemical studies of localization and co-localization of glutamate, aspartate and GABA in the anterior thalamic nuclei, retrosplenial granular cortex, thalamic reticular nucleus and mammillary nuclei of the rat. J Chem Neuroanat 12:77–84

    Article  CAS  PubMed  Google Scholar 

  29. De Biasi S, Arcelli P, Spreafico R (1997) Parvalbumin immunoreactivity in the thalamus of guinea pig: light and electron microscopic correlation with gamma-aminobutyric acid immunoreactivity. J Comp Neurol 348:556–569

    Article  Google Scholar 

  30. Fritschy JM, Mohler H (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154–194

    Article  CAS  PubMed  Google Scholar 

  31. Chu DC, Albin RL, Young AB, Penney JB (1990) Distribution and kinetics of GABAB binding sites in rat central nervous system: a quantitative autoradiographic study. Neuroscience 34:341–357

    Article  CAS  PubMed  Google Scholar 

  32. Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040–1062

    CAS  PubMed  Google Scholar 

  33. Steriade M, Parent A, Hada J (1984) Thalamic projections of nucleus reticularis thalami of cat: a study using retrograde transport of horseradish peroxidase and fluorescent tracers. J Comp Neurol 229:531–547

    Article  CAS  PubMed  Google Scholar 

  34. Paré D, Steriade M, Deschêenes M, Oakson G (1987) Physiological characteristics of anterior thalamic nuclei, a group devoid of inputs from reticular thalamic nucleus. J Neurophysiol 57:1669–1685

    PubMed  Google Scholar 

  35. Madarász M, Somogyi G, Somogyi J, Hámori J (1985) Numerical estimation of gamma-aminobutyric acid (GABA)-containing neurons in three thalamic nuclei of the cat: direct GABA immunocytochemistry. Neurosci Lett 61:73–78

    Article  PubMed  Google Scholar 

  36. Rinvik E, Ottersen OP, Storm-Mathisen J (1987) Gamma-aminobutyrate-like immunoreactivity in the thalamus of the cat. Neuroscience 21:781–805

    Article  CAS  PubMed  Google Scholar 

  37. Kultas-Ilinsky K, Yi H, Ilinsky IA (1995) Nucleus reticularis thalami input to the anterior thalamic nuclei in the monkey: a light and electron microscopic study. Neurosci Lett 186:25–28

    Article  CAS  PubMed  Google Scholar 

  38. Smith Y, Séguéla P, Parent A (1987) Distribution of GABA-immunoreactive neurons in the thalamus of the squirrel monkey (Saimiri sciureus). Neuroscience 22:579–591

    Article  CAS  PubMed  Google Scholar 

  39. Hunt CA, Pang DZ, Jones EG (1991) Distribution and density of GABA cells in intralaminar and adjacent nuclei of monkey thalamus. Neuroscience 43:185–196

    Article  CAS  PubMed  Google Scholar 

  40. Benson DL, Isackson PJ, Hendry SH, Jones EG (1991) Differential gene expression for glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase in basal ganglia, thalamus, and hypothalamus of the monkey. J Neurosci 11:1540–1564

    CAS  PubMed  Google Scholar 

  41. Huntsman MM, Leggio MG, Jones EG (1996) Nucleus-specific expression of GABA(A) receptor subunit mRNAs in monkey thalamus. J Neurosci 16:3571–3589

    CAS  PubMed  Google Scholar 

  42. Muñoz A, Huntsman MM, Jones EG (1998) GABA(B) receptor gene expression in monkey thalamus. J Comp Neurol 394:118–126

    Article  PubMed  Google Scholar 

  43. Dixon G, Harper CG (2001) Quantitative analysis of glutamic acid decarboxylase-immunoreactive neurons in the anterior thalamus of the human brain. Brain Res 923:39–44

    Article  CAS  PubMed  Google Scholar 

  44. Popken GJ, Leggio MG, Bunney WE Jr, Jones EG (2002) Expression of mRNAs related to the GABAergic and glutamatergic neurotransmitter systems in the human thalamus: normal and schizophrenic. Thalamus Relat Syst 1:349–369

    Article  CAS  Google Scholar 

  45. Arcelli P, Frassoni C, Regondi MC, De Biasi S, Spreafico R (1997) GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Res Bull 42:27–37

    Article  CAS  PubMed  Google Scholar 

  46. McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex. J Clin Neurophysiol 9:212–223

    Article  CAS  PubMed  Google Scholar 

  47. Salt TE, Eaton SA (1996) Functions of ionotropic and metabotropic glutamate receptors in sensory transmission in the mammalian thalamus. Prog Neurobiol 48:55–72

    Article  CAS  PubMed  Google Scholar 

  48. Baughman RW, Gilbert CD (1981) Aspartate and glutamate as possible neurotransmitters of cells in layer 6 of the visual cortex. Nature 287:848–850

    Article  Google Scholar 

  49. McCormick DA, von Krosigk M (1992) Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proc Natl Acad Sci U S A 89:2774–2778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Broman J (1994) Neurotransmitters in subcortical somatosensory pathways. Anat Embryol (Berl) 189:181–214

    Article  CAS  Google Scholar 

  51. Golshani P, Warren RA, Jones EG (1998) Progression of change in NMDA, non-NMDA, and metabotropic glutamate receptor function at the developing corticothalamic synapse. J Neurophysiol 80:143–154

    CAS  PubMed  Google Scholar 

  52. Mayer ML, Westbrook GL (1987) The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol 28:197–276

    Article  CAS  PubMed  Google Scholar 

  53. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31–108

    Article  CAS  PubMed  Google Scholar 

  54. Nakanishi S (1994) Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 13:1031–1037

    Article  CAS  PubMed  Google Scholar 

  55. Herring BE, Silm K, Edwards RH, Nicoll RA (2015) Is aspartate an excitatory neurotransmitter? J Neurosci 35:10168–10171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kubrusly RC, de Mello MC, de Mello FG (1998) Aspartate as a selective NMDA receptor agonist in cultured cells from the avian retina. Neurochem Int 32:47–52

    Article  CAS  PubMed  Google Scholar 

  57. Gundersen V, Chaudhry FA, Bjaalie JG, Fonnum F, Ottersen OP, Storm-Mathisen J (1998) Synaptic vesicular localization and exocytosis of L-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J Neurosci 18:6059–6070

    CAS  PubMed  Google Scholar 

  58. Cavallero A, Marte A, Fedele E (2009) L-aspartate as an amino acid neurotransmitter: mechanisms of the depolarization-induced release from cerebrocortical synaptosomes. J Neurochem 110:924–934

    Article  CAS  PubMed  Google Scholar 

  59. Tsumoto T (1990) Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral neocortex. Neurosci Res 9:79–102

    Article  CAS  PubMed  Google Scholar 

  60. Hicks TP, Kaneko T, Metherate R, Oka JI, Stark CA (1991) Amino acids as transmitters of synaptic excitation in neocortical sensory processes. Can J Physiol Pharmacol 69:1099–1114

    Article  CAS  PubMed  Google Scholar 

  61. Johnson RR, Burkhalter A (1992) Evidence for excitatory amino acid neurotransmitters in the geniculo-cortical pathway and local projections within rat primary visual cortex. Exp Brain Res 89:20–30

    Article  CAS  PubMed  Google Scholar 

  62. Kharazia VN, Weinberg RJ (1994) Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex. J Neurosci 14:6021–6032

    CAS  PubMed  Google Scholar 

  63. Wang B, Gonzalo-Ruiz A, Sanz JM, Campbell G, Lieberman AR (2001) Glutamatergic components of the retrosplenial granular cortex in the rat. J Neurocytol 30:427–441

    Article  CAS  PubMed  Google Scholar 

  64. Seki M, Zyo K (1984) Anterior thalamic afferents from the mamillary body and the limbic cortex in the rat. J Comp Neurol 229:242–256

    Article  CAS  PubMed  Google Scholar 

  65. Van Groen T, Wyss JM (1990) Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 300:593–606

    Article  CAS  PubMed  Google Scholar 

  66. Van Groen T, Wyss JM (1995) Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J Comp Neurol 358:584–604

    Article  CAS  PubMed  Google Scholar 

  67. Van Groen T, Wyss JM (2003) Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:249–263

    Article  PubMed  Google Scholar 

  68. Shibata H (1993) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol 337:431–445

    Article  CAS  PubMed  Google Scholar 

  69. Shibata H, Kato A (1993) Topographic relationship between anteromedial thalamic nucleus neurons and their cortical terminal fields in the rat. Neurosci Res 17:63–69

    Article  CAS  PubMed  Google Scholar 

  70. Van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Brain Res Rev 30:1–26

    Article  CAS  PubMed  Google Scholar 

  71. Shibata H, Naito J (2005) Organization of anterior cingulate and frontal cortical projections to the anterior and laterodorsal thalamic nuclei in the rat. Brain Res 1059:93–103

    Article  CAS  PubMed  Google Scholar 

  72. Wright NF, Erichsen JT, Vann SD, O’Mara SM, Aggleton JP (2010) Parallel but separate inputs from limbic cortices to the mammillary bodies and anterior thalamic nuclei in the rat. J Comp Neurol 518:2334–2354

    Article  PubMed  PubMed Central  Google Scholar 

  73. Gonzalo-Ruiz A, Sanz JM, Morte L, Lieberman AR (1997) Glutamate and aspartate immunoreactivity in the reciprocal projections between the anterior thalamic nuclei and the retrosplenial granular cortex in the rat. Brain Res Bull 42:309–321

    Article  CAS  PubMed  Google Scholar 

  74. Gonzalo-Ruiz A, Morte L, Lieberman AR (1997) Evidence for collateral projections to the retrosplenial granular cortex and thalamic reticular nucleus from glutamate and/or aspartate-containing neurons of the anterior thalamic nuclei in the rat. Exp Brain Res 116:63–72

    Article  CAS  PubMed  Google Scholar 

  75. Gonzalo-Ruiz A, Morte L, Sanz JM (1998) Glutamate/aspartate and leu-enkephalin immunoreactivity in mammillothalamic projection neurons of the rat. Brain Res Bull 47:565–574

    Article  CAS  PubMed  Google Scholar 

  76. Vann SD, Saunders RC, Aggleton JP (2007) Distinct, parallel pathways link the medial mammillary bodies to the anterior thalamus in macaque monkeys. Eur J Neurosci 26:1575–1586

    Article  PubMed  Google Scholar 

  77. Watanabe K, Kawana E (1980) A horseradish peroxidase study on the mammillothalamic tract in the rat. Acta Anat (Basel) 108:394–401

    Article  CAS  Google Scholar 

  78. Shibata H (1992) Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat. J Comp Neurol 323:117–127

    Article  CAS  PubMed  Google Scholar 

  79. McEntee WJ, Crook TH (1993) Glutamate: its role in learning, memory, and the aging brain. Psychopharmacology 111:391–401

    Article  CAS  PubMed  Google Scholar 

  80. Riedel G, Platt B, Micheau J (2003) Glutamate receptor function in learning and memory. Behav Brain Res 140:1–47

    Article  CAS  PubMed  Google Scholar 

  81. Reis HJ, Guatimosim C, Paquet M, Santos M, Ribeiro FM, Kummer A, Schenatto G, Salgado JV, Vieira LB, Teixeira AL, Palotás A (2009) Neuro-transmitters in the central nervous system & their implication in learning and memory processes. Curr Med Chem 16:796–840

    Article  CAS  PubMed  Google Scholar 

  82. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, Erickson JD, Liu G (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT. J Neurosci 25:6221–6234

    Article  CAS  PubMed  Google Scholar 

  83. Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98–103

    Article  CAS  PubMed  Google Scholar 

  84. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983–1002

    Article  CAS  PubMed  Google Scholar 

  85. Barroso-Chinea P, Castle M, Aymerich MS, Pérez-Manso M, Erro E, Tuñon T, Lanciego JL (2007) Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. J Comp Neurol 501:703–715

    Article  CAS  PubMed  Google Scholar 

  86. Oda S, Funato H, Sato F, Adachi-Akahane S, Ito M, Takase K, Kuroda M (2014) A subset of thalamocortical projections to the retrosplenial cortex possesses two vesicular glutamate transporter isoforms, VGluT1 and VGluT2, in axon terminals and somata. J Comp Neurol 522:2089–2106

    Article  CAS  PubMed  Google Scholar 

  87. Schuske K, Jorgensen EM (2004) Vesicular glutamate transporter—shooting blanks science. Neuroscience 304:1750–1752

    CAS  Google Scholar 

  88. Goodridge JP, Taube JS (1997) Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17:9315–9330

    CAS  PubMed  Google Scholar 

  89. Hargreaves EL, Yoganarasimha D, Knierim JJ (2007) Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex, and hippocampus. Hippocampus 17:826–841

    Article  PubMed  Google Scholar 

  90. Taube JS, Bassett JP (2003) Persistent neural activity in head direction cells. Cereb Cortex 13:1162–1172

    Article  PubMed  Google Scholar 

  91. Clark BJ, Bassett JP, Wang SS, Taube JS (2010) Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J Neurosci 30:5289–5302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Buller AL, Larson HC, Schneider BE, Beaton JA, Morrisett RA, Monaghan DT (1994) The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition. J Neurosci 14:5471–5484

    CAS  PubMed  Google Scholar 

  93. Martin LJ, Blackstone CD, Levey AI, Huganir RL, Price DL (1993) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53:327–358

    Article  CAS  PubMed  Google Scholar 

  94. Sato K, Kiyama H, Tohyama M (1993) The differential expression patterns of messenger RNAs encoding non-N-methyl-D-aspartate glutamate receptor subunits (GluR1-4) in the rat brain. Neuroscience 52:515–539

    Article  CAS  PubMed  Google Scholar 

  95. Spreafico R, Frassoni C, Arcelli P, Battaglia G, Wenthold RJ, De Biasi S (1994) Distribution of AMPA selective glutamate receptors in the thalamus of adult rats and during postnatal development. A light and ultrastructural immunocytochemical study. Brain Res Dev Brain Res 82:231–244

    Article  CAS  PubMed  Google Scholar 

  96. Gold SJ, Ambros-Ingerson J, Horowitz JR, Lynch G, Gall CM (1997) Stoichiometries of AMPA receptor subunit mRNAs in rat brain fall into discrete categories. J Comp Neurol 385:491–502

    Article  CAS  PubMed  Google Scholar 

  97. Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582–3598

    CAS  PubMed  Google Scholar 

  98. Banay-Schwartz M, Lajtha A, Palkovits M (1992) Regional distribution of glutamate and aspartate in adult and old human brain. Brain Res 594:343–346

    Article  CAS  PubMed  Google Scholar 

  99. Jones EG, Huntley GW, Benson DL (1994) Alpha calcium/calmodulin-dependent protein kinase II selectively expressed in a subpopulation of excitatory neurons in monkey sensory-motor cortex: comparison with GAD-67 expression. J Neurosci 14:611–629

    CAS  PubMed  Google Scholar 

  100. Tighilet B, Huntsman MM, Hashikawa T, Murray KD, Isackson PJ, Jones EG (1998) Cell-specific expression of type II calcium/calmodulin-dependent protein kinase isoforms and glutamate receptors in normal and visually deprived lateral geniculate nucleus of monkeys. J Comp Neurol 390:278–296

    Article  CAS  PubMed  Google Scholar 

  101. Jones EG, Tighilet B, Tran BV, Huntsman MM (1998) Nucleus- and cell-specific expression of NMDA and non-NMDA receptor subunits in monkey thalamus. J Comp Neurol 397:371–393

    Article  CAS  PubMed  Google Scholar 

  102. Ibrahim HM, Healy DJ, Hogg AJ Jr, Meador-Woodruff JH (2000) Nucleus-specific expression of ionotropic glutamate receptor subunit mRNAs and binding sites in primate thalamus. Brain Res Mol Brain Res 79:1–17

    Article  CAS  PubMed  Google Scholar 

  103. Woolf NJ, Butcher LL (1986) Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603–637

    Article  CAS  PubMed  Google Scholar 

  104. Woolf NJ (1991) Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475–524

    Article  CAS  PubMed  Google Scholar 

  105. Darvesh S, Grantham DL, Hopkins DA (1998) Distribution of butyrylcholinesterase in the human amygdala and hippocampal formation. J Comp Neurol 393:374–390

    Article  CAS  PubMed  Google Scholar 

  106. Darvesh S, Hopkins DA, Geula C (2003) Neurobiology of butyrylcholinesterase. Nat Rev Neurosci 4:131–138

    Article  CAS  PubMed  Google Scholar 

  107. Mesulam M, Guillozet A, Shaw P, Quinn B (2002) Widely spread butyrylcholinesterase can hydrolyze acetylcholine in the normal and Alzheimer brain. Neurobiol Dis 9:88–93

    Article  CAS  PubMed  Google Scholar 

  108. Duysen EG, Li B, Darvesh S, Lockridge O (2007) Sensitivity of butyrylcholinesterase knockout mice to (−)-huperzine A and donepezil suggests humans with butyrylcholinesterase deficiency may not tolerate these Alzheimer’s disease drugs and indicates butyrylcholinesterase function in neurotransmission. Toxicology 233:60–69

    Article  CAS  PubMed  Google Scholar 

  109. Eglen RM (2006) Muscarinic receptor subtypes in neuronal and non-neuronal cholinergic function. Auton Autocoid Pharmacol 26:219–233

    Article  CAS  Google Scholar 

  110. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Tago H, Maeda T, McGeer PL, Kimura H (1992) Butyrylcholinesterase-rich neurons in rat brain demonstrated by a sensitive histochemical method. J Comp Neurol 325:301–312

    Article  CAS  PubMed  Google Scholar 

  112. Levey AI, Hallanger AE, Wainer BH (1987) Choline acetyltransferase immunoreactivity in the rat thalamus. J Comp Neurol 257:317–332

    Article  CAS  PubMed  Google Scholar 

  113. Gonzalo-Ruiz A, Sanz-Anquela MJ, Lieberman AR (1995) Cholinergic projections to the anterior thalamic nuclei in the rat: a combined retrograde tracing and choline acetyl transferase immunohistochemical study. Anat Embryol (Berl) 192:335–349

    Article  CAS  Google Scholar 

  114. Ichikawa T, Ajiki K, Matsuura J, Misawa H (1997) Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J Chem Neuroanat 13:23–39

    Article  CAS  PubMed  Google Scholar 

  115. Roghani A, Shirzadi A, Butcher LL, Edwards RH (1998) Distribution of the vesicular transporter for acetylcholine in the rat central nervous system. Neuroscience 82:1195–1212

    Article  CAS  PubMed  Google Scholar 

  116. Holmstrand EC, Asafu-Adjei J, Sampson AR, Blakely RD, Sesack SR (2010) Ultrastructural localization of high-affinity choline transporter in the rat anteroventral thalamus and ventral tegmental area: differences in axon morphology and transporter distribution. J Comp Neurol 518:1908–1924

    Article  PubMed  PubMed Central  Google Scholar 

  117. Schwartz RD (1986) Autoradiographic distribution of high affinity muscarinic and nicotinic cholinergic receptors labeled with [3H]acetylcholine in rat brain. Life Sci 38:2111–2119

    Article  CAS  PubMed  Google Scholar 

  118. Buckley NJ, Bonner TI, Brann MR (1988) Localization of a family of muscarinic receptor mRNAs in rat brain. J Neurosci 8:4646–4652

    CAS  PubMed  Google Scholar 

  119. Amadeo A, Arcelli P, Spreafico R, De Biasi S (1995) Ultrastructural immunolocalization of muscarinic acetylcholine receptor in the dorsal thalamus of rat. Neurosci Lett 184:161–164

    Article  CAS  PubMed  Google Scholar 

  120. Sikes RW, Vogt BA (1987) Afferent connections of anterior thalamus in rats: sources and association with muscarinic acetylcholine receptors. J Comp Neurol 256:538–551

    Article  CAS  PubMed  Google Scholar 

  121. Clarke PB, Schwartz RD, Paul SM, Pert CB, Pert A (1985) Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]-alpha-bungarotoxin. J Neurosci 5:1307–1315

    CAS  PubMed  Google Scholar 

  122. Steriade M, Paré D, Parent A, Smith Y (1988) Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey. Neuroscience 25:47–67

    Article  CAS  PubMed  Google Scholar 

  123. Olivier A, Parent A, Poirier LJ (1970) Identification of the thalamic nuclei on the basis of their cholinesterase content in the monkey. J Anat 106:37–50

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Darvesh S, Hopkins DA (2003) Differential distribution of butyrylcholinesterase and acetylcholinesterase in the human thalamus. J Comp Neurol 463:25–43

    Article  CAS  PubMed  Google Scholar 

  125. Heckers S, Geula C, Mesulam MM (1992) Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J Comp Neurol 325:68–82

    Article  CAS  PubMed  Google Scholar 

  126. Adem A, Jossan SS, d’Argy R, Brandt I, Winblad B, Nordberg A (1988) Distribution of nicotinic receptors in human thalamus as visualized by 3H-nicotine and 3H-acetylcholine receptor autoradiography. J Neural Transm 73:77–83

    Article  CAS  PubMed  Google Scholar 

  127. Spurden DP, Court JA, Lloyd S, Oakley A, Perry R, Pearson C, Pullen RG, Perry EK (1997) Nicotinic receptor distribution in the human thalamus: autoradiographical localization of [3H]nicotine and [125I] alpha-bungarotoxin binding. J Chem Neuroanat 13:105–113

    Article  CAS  PubMed  Google Scholar 

  128. Han ZY, Zoli M, Cardona A, Bourgeois JP, Changeux JP, Le Novère N (2003) Localization of [3H]nicotine, [3H]cytisine, [3H]epibatidine, and [125I]alpha-bungarotoxin binding sites in the brain of Macaca mulatta. J Comp Neurol 461:49–60

    Article  CAS  PubMed  Google Scholar 

  129. Cortés R, Probst A, Tobler HJ, Palacios JM (1986) Muscarinic cholinergic receptor subtypes in the human brain. II. Quantitative autoradiographic studies. Brain Res 362:239–523

    Article  PubMed  Google Scholar 

  130. Hoover DB, Baisden RH (1980) Localization of putative cholinergic neurons innervating the anteroventral thalamus. Brain Res Bull 5:519–524

    Article  CAS  PubMed  Google Scholar 

  131. Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262:105–124

    Article  CAS  PubMed  Google Scholar 

  132. Holmstrand EC, Sesack SR (2011) Projections from the rat pedunculopontine and laterodorsal tegmental nuclei to the anterior thalamus and ventral tegmental area arise from largely separate populations of neurons. Brain Struct Funct 216:331–345

    Article  PubMed  PubMed Central  Google Scholar 

  133. Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641–667

    Article  CAS  PubMed  Google Scholar 

  134. Moore RY, Halaris AE, Jones BE (1978) Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol 180:417–438

    Article  CAS  PubMed  Google Scholar 

  135. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083–1152

    Article  CAS  PubMed  Google Scholar 

  136. Cropper EC, Eisenman JS, Azmitia EC (1984) An immunocytochemical study of the serotonergic innervation of the thalamus of the rat. J Comp Neurol 224:38–50

    Article  CAS  PubMed  Google Scholar 

  137. Gonzalo-Ruiz A, Lieberman AR, Sanz-Anquela JM (1995) Organization of serotoninergic projections from the raphé nuclei to the anterior thalamic nuclei in the rat: a combined retrograde tracing and 5-HT immunohistochemical study. J Chem Neuroanat 8:103–115

    Article  CAS  PubMed  Google Scholar 

  138. Vertes RP, Linley SB, Hoover WB (2010) Pattern of distribution of serotonergic fibers to the thalamus of the rat. Brain Struct Funct 215:1–28

    Article  CAS  PubMed  Google Scholar 

  139. Nielsen K, Brask D, Knudsen GM, Aznar S (2006) Immunodetection of the serotonin transporter protein is a more valid marker for serotonergic fibers than serotonin. Synapse 59:270–276

    Article  CAS  PubMed  Google Scholar 

  140. Lavoie B, Parent A (1991) Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J Comp Neurol 312:1–18

    Article  CAS  PubMed  Google Scholar 

  141. Gustafson EL, Durkin MM, Bard JA, Zgombick J, Branchek TA (1996) A receptor autoradiographic and in situ hybridization analysis of the distribution of the 5-ht7 receptor in rat brain. Br J Pharmacol 117:657–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Kinsey AM, Wainwright A, Heavens R, Sirinathsinghji DJ, Oliver KR (2001) Distribution of 5-ht(5 A), 5-ht(5B), 5-ht(6) and 5-HT(7) receptor mRNAs in the rat brain. Brain Res Mol Brain Res 88:194–198

    Article  CAS  PubMed  Google Scholar 

  143. Neumaier JF, Sexton TJ, Yracheta J, Diaz AM, Brownfield M (2001) Localization of 5-HT(7) receptors in rat brain by immunocytochemistry, in situ hybridization, and agonist stimulated cFos expression. J Chem Neuroanat 21:63–73

    Article  CAS  PubMed  Google Scholar 

  144. Bruinvels AT, Palacios JM, Hoyer D (1993) Autoradiographic characterisation and localisation of 5-HT1D compared to 5-HT1B binding sites in rat brain. Naunyn Schmiedeberg’s Arch Pharmacol 347:569–582

    Article  CAS  Google Scholar 

  145. Ward RP, Hamblin MW, Lachowicz JE, Hoffman BJ, Sibley DR, Dorsa DM (1995) Localization of serotonin subtype 6 receptor messenger RNA in the rat brain by in situ hybridization histochemistry. Neuroscience 64:1105–1111

    Article  CAS  PubMed  Google Scholar 

  146. Oliver KR, Kinsey AM, Wainwright A, Sirinathsinghji DJ (2000) Localization of 5-ht(5A) receptor-like immunoreactivity in the rat brain. Brain Res 867:131–142

    Article  CAS  PubMed  Google Scholar 

  147. Martín-Cora FJ, Pazos A (2004) Autoradiographic distribution of 5-HT7 receptors in the human brain using [3H]mesulergine: comparison to other mammalian species. Br J Pharmacol 141:92–104

    Article  PubMed  CAS  Google Scholar 

  148. Varnäs K, Thomas DR, Tupala E, Tiihonen J, Hall H (2004) Distribution of 5-HT7 receptors in the human brain: a preliminary autoradiographic study using [3H]SB-269970. Neurosci Lett 367:313–316

    Article  PubMed  CAS  Google Scholar 

  149. Meneses A (2014) Memory formation and memory alterations: 5-HT6 and 5-HT7 receptors, novel alternative. Rev Neurosci 25:325–356

    CAS  PubMed  Google Scholar 

  150. Stiedl O, Pappa E, Konradsson-Geuken Å, Ögren SO (2015) The role of the serotonin receptor subtypes 5-HT1A and 5-HT7 and its interaction in emotional learning and memory. Front Pharmacol 6:162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  151. Chapin EM, Andrade R (2001) A 5-HT(7) receptor-mediated depolarization in the anterodorsal thalamus. II. Involvement of the hyperpolarization-activated current I(h). J Pharmacol Exp Ther 297:403–409

    CAS  PubMed  Google Scholar 

  152. Varnäs K, Halldin C, Pike VW, Hall H (2003) Distribution of 5-HT4 receptors in the postmortem human brain—an autoradiographic study using [125I]SB 207710. Eur Neuropsychopharmacol 13:228–234

    Article  PubMed  CAS  Google Scholar 

  153. Spitzer NC, Borodinsky LN, Root CM (2005) Homeostatic activity-dependent paradigm for neurotransmitter specification. Cell Calcium 37:417–423

    Article  CAS  PubMed  Google Scholar 

  154. Neveu D, Zucker RS (1996) Postsynaptic levels of [Ca2+]i needed to trigger LTD and LTP. Neuron 16:619–629

    Article  CAS  PubMed  Google Scholar 

  155. Yang SN, Tang YG, Zucker RS (1999) Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol 81:781–787

    CAS  PubMed  Google Scholar 

  156. Komuro H, Kumada T (2005) Ca2+ transients control CNS neuronal migration. Cell Calcium 37:387–393

    Article  CAS  PubMed  Google Scholar 

  157. Fields RD, Lee PR, Cohen JE (2005) Temporal integration of intracellular Ca2+ signaling networks in regulating gene expression by action potentials. Cell Calcium 37:433–442

    Article  CAS  PubMed  Google Scholar 

  158. Hardingham GE, Bading H (1998) Nuclear calcium: a key regulator of gene expression. Biometals 11:345–358

    Article  CAS  PubMed  Google Scholar 

  159. Bennett MR, Huxlin KR (1996) Neuronal cell death in the mammalian nervous system: the calmortin hypothesis. Gen Pharmacol 27:407–419

    Article  CAS  PubMed  Google Scholar 

  160. Krebs J (1998) The role of calcium in apoptosis. Biometals 11:375–382

    Article  CAS  PubMed  Google Scholar 

  161. Rogers JH (1987) Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J Cell Biol 105:1343–1353

    Article  CAS  PubMed  Google Scholar 

  162. Faas GC, Schwaller B, Vergara JL, Mody I (2007) Resolving the fast kinetics of cooperative binding: Ca2+ buffering by calretinin. PLoS Biol 5:e311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  163. Schwaller B (2009) The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 66:275–300

    Article  CAS  PubMed  Google Scholar 

  164. Berggård T, Miron S, Onnerfjord P, Thulin E, Åkerfeldt KS, Enghild JJ, Akke M, Linse S (2002) Calbindin D28k exhibits properties characteristic of a Ca2+ sensor. J Biol Chem 277:16662–16672

    Article  PubMed  CAS  Google Scholar 

  165. Billing-Marczak K, Kuźnicki J (1999) Calretinin—sensor or buffer—function still unclear. Pol J Pharmacol 51:173–178

    CAS  PubMed  Google Scholar 

  166. Schwaller B, Durussel I, Jermann D, Herrmann B, Cox JA (1997) Comparison of the Ca2+-binding properties of human recombinant calretinin-22k and calretinin. J Biol Chem 272:29663–29671

    Article  CAS  PubMed  Google Scholar 

  167. D’Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, Gotzos V, Celio MR (2001) Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 909:145–158

    Article  PubMed  Google Scholar 

  168. D’Orlando C, Celio MR, Schwaller B (2002) Calretinin and calbindin D-28 k, but not parvalbumin protect against glutamate-induced delayed excitotoxicity in transfected N18-RE 105 neuroblastoma-retina hybrid cells. Brain Res 945:181–190

    Article  PubMed  Google Scholar 

  169. Lukas W, Jones KA (1994) Cortical neurons containing calretinin are selectively resistant to calcium overload and excitotoxicity in vitro. Neuroscience 61:307–316

    Article  CAS  PubMed  Google Scholar 

  170. Yenari MA, Minami M, Sun GH, Meier TJ, Kunis DM, McLaughlin JR, Ho DY, Sapolsky RM, Steinberg GK (2001) Calbindin d28k overexpression protects striatal neurons from transient focal cerebral ischemia. Stroke 32:1028–1035

    Article  CAS  PubMed  Google Scholar 

  171. Yuan HH, Chen RJ, Zhu YH, Peng CL, Zhu XR (2012) The neuroprotective effect of overexpression of calbindin-D(28k) in an animal model of Parkinson’s disease. Mol Neurobiol 47:117–122

    Article  PubMed  CAS  Google Scholar 

  172. Molinari S, Battini R, Ferrari S, Pozzi L, Killcross AS, Robbins TW, Jouvenceau A, Billard JM, Dutar P, Lamour Y, Baker WA, Cox H, Emson PC (1996) Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D28K expression. Proc Natl Acad Sci U S A 93:8028–8033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Schurmans S, Schiffmann SN, Gurden H, Lemaire M, Lipp HP, Schwam V, Pochet R, Imperato A, Böhme GA, Parmentier M (1997) Impaired long-term potentiation induction in dentate gyrus of calretinin-deficient mice. Proc Natl Acad Sci U S A 94:10415–10420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Jouvenceau A, Potier B, Battini R, Ferrari S, Dutar P, Billard JM (1999) Glutamatergic synaptic responses and long-term potentiation are impaired in the CA1 hippocampal area of calbindin D(28k)-deficient mice. Synapse 33:172–180

    Article  CAS  PubMed  Google Scholar 

  175. Gall D, Roussel C, Susa I, D’Angelo E, Rossi P, Bearzatto B, Galas MC, Blum D, Schurmans S, Schiffmann SN (2003) Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin. J Neurosci 23:9320–9327

    CAS  PubMed  Google Scholar 

  176. Abrahám H, Orsi G, Seress L (2007) Ontogeny of cocaine- and amphetamine-regulated transcript (CART) peptide and calbindin immunoreactivity in granule cells of the dentate gyrus in the rat. Int J Dev Neurosci 25:265–274

    Article  PubMed  CAS  Google Scholar 

  177. Murray KD, Choudary PV, Jones EG (2007) Nucleus- and cell-specific gene expression in monkey thalamus. Proc Natl Acad Sci U S A 104:1989–1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Camp AJ, Wijesinghe R (2009) Calretinin: modulator of neuronal excitability. Int J Biochem Cell Biol 41:2118–2121

    Article  CAS  PubMed  Google Scholar 

  179. Schwaller B (2014) Calretinin: from a “simple” Ca(2+) buffer to a multifunctional protein implicated in many biological processes. Front Neuroanat 8:3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  180. Jones EG, Hendry SH (1989) Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1:222–246

    Article  PubMed  Google Scholar 

  181. Molinari M, Dell’Anna ME, Rausell E, Leggio MG, Hashikawa T, Jones EG (1995) Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity. J Comp Neurol 362:171–194

    Article  CAS  PubMed  Google Scholar 

  182. Nitsch C, Scotti A, Sommacal A, Kalt G (1989) GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2+ binding protein parvalbumin. Neurosci Lett 105:263–268

    Article  CAS  PubMed  Google Scholar 

  183. Waldvogel HJ, Faull RL, Williams MN, Dragunow M (1991) Differential sensitivity of calbindin and parvalbumin immunoreactive cells in the striatum to excitotoxins. Brain Res 546:329–335

    Article  CAS  PubMed  Google Scholar 

  184. Dávila JC, Real MA, Olmos L, Legaz I, Medina L, Guirado S (2005) Embryonic and postnatal development of GABA, calbindin, calretinin, and parvalbumin in the mouse claustral complex. J Comp Neurol 481:42–57

    Article  PubMed  Google Scholar 

  185. Grateron L, Cebada-Sanchez S, Marcos P, Mohedano-Moriano A, Insausti AM, Muñoz M, Arroyo-Jimenez MM, Martinez-Marcos A, Artacho-Perula E, Blaizot X, Insausti R (2003) Postnatal development of calcium-binding proteins immunoreactivity (parvalbumin, calbindin, calretinin) in the human entorhinal cortex. J Chem Neuroanat 26:311–316

    Article  CAS  PubMed  Google Scholar 

  186. Kishimoto J, Tsuchiya T, Cox H, Emson PC, Nakayama Y (1998) Age-related changes of calbindin-D28k, calretinin, and parvalbumin mRNAs in the hamster brain. Neurobiol Aging 19:77–82

    Article  CAS  PubMed  Google Scholar 

  187. Yew DT, Luo CB, Heizmann CW, Chan WY (1997) Differential expression of calretinin, calbindin D28K and parvalbumin in the developing human cerebellum. Brain Res Dev Brain Res 103:37–45

    Article  CAS  PubMed  Google Scholar 

  188. Bernstein HG, Krause S, Krell D, Dobrowolny H, Wolter M, Stauch R, Ranft K, Danos P, Jirikowski GF, Bogerts B (2007) Strongly reduced number of parvalbumin-immunoreactive projection neurons in the mammillary bodies in schizophrenia: further evidence for limbic neuropathology. Ann N Y Acad Sci 1096:120–127

    Article  CAS  PubMed  Google Scholar 

  189. Danos P, Baumann B, Bernstein HG, Franz M, Stauch R, Northoff G, Krell D, Falkai P, Bogerts B (1998) Schizophrenia and anteroventral thalamic nucleus: selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons. Psychiatry Res 82:1–10

    Article  CAS  PubMed  Google Scholar 

  190. Mikkonen M, Alafuzoff I, Tapiola T, Soininen H, Miettinen R (1999) Subfield- and layer-specific changes in parvalbumin, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer’s disease. Neuroscience 92:515–532

    Article  CAS  PubMed  Google Scholar 

  191. Yamada T, McGeer PL, Baimbridge KG, McGeer EG (1990) Relative sparing in Parkinson’s disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res 526:303–307

    Article  CAS  PubMed  Google Scholar 

  192. Résibois A, Rogers JH (1992) Calretinin in rat brain: an immunohistochemical study. Neuroscience 46:101–134

    Article  PubMed  Google Scholar 

  193. Winsky L, Montpied P, Arai R, Martin BM, Jacobowitz DM (1992) Calretinin distribution in the thalamus of the rat: immunohistochemical and in situ hybridization histochemical analyses. Neuroscience 50:181–196

    Article  CAS  PubMed  Google Scholar 

  194. Arai R, Jacobowitz DM, Deura S (1994) Distribution of calretinin, calbindin-D28k, and parvalbumin in the rat thalamus. Brain Res Bull 33:595–614

    Article  CAS  PubMed  Google Scholar 

  195. Frassoni C, Arcelli P, Selvaggio M, Spreafico R (1998) Calretinin immunoreactivity in the developing thalamus of the rat: a marker of early generated thalamic cells. Neuroscience 83:1203–1214

    Article  CAS  PubMed  Google Scholar 

  196. Fan X, Warner M, Gustafsson JA (2006) Estrogen receptor beta expression in the embryonic brain regulates development of calretinin-immunoreactive GABAergic interneurons. Proc Natl Acad Sci U S A 103:19338–19343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Żakowski W, Robak A (2013) Developmental changes of calretinin immunoreactivity in the anterior thalamic nuclei of the guinea pig. J Chem Neuroanat 47:28–34

    Article  PubMed  CAS  Google Scholar 

  198. Abbott LC, Jacobowitz DM (1995) Development of calretinin-immunoreactive unipolar brush-like cells and an afferent pathway to the embryonic and early postnatal mouse cerebellum. Anat Embryol (Berl) 191:541–559

    Article  CAS  Google Scholar 

  199. Abbott LC, Jacobowitz DM (1999) Developmental expression of calretinin-immunoreactivity in the thalamic eminence of the fetal mouse. Int J Dev Neurosci 17:331–345

    Article  CAS  PubMed  Google Scholar 

  200. Fonseca M, dél Río JA, Martínez A, Gómez S, Soriano E (1995) Development of calretinin immunoreactivity in the neocortex of the rat. J Comp Neurol 361:177–192.

  201. Guandalini P (2001) The efferent connections to the thalamus and brainstem of the physiologically defined eye field in the rat medial frontal cortex. Brain Res Bull 54:175–186

    Article  CAS  PubMed  Google Scholar 

  202. Fortin M, Asselin MC, Parent A (1996) Calretinin immunoreactivity in the thalamus of the squirrel monkey. J Chem Neuroanat 10:101–117

    Article  CAS  PubMed  Google Scholar 

  203. Alelú-Paz R, Giménez-Amaya JM (2007) Chemical parcellation of the anterior thalamic nuclei in the human brain. J Neural Transm 114:969–981

    Article  PubMed  CAS  Google Scholar 

  204. Fortin M, Asselin MC, Gould PV, Parent A (1998) Calretinin-immunoreactive neurons in the human thalamus. Neuroscience 84:537–548

    Article  CAS  PubMed  Google Scholar 

  205. Münkle MC, Waldvogel HJ, Faull RL (2000) The distribution of calbindin, calretinin and parvalbumin immunoreactivity in the human thalamus. J Chem Neuroanat 19:155–173

    Article  PubMed  Google Scholar 

  206. Morel A, Magnin M, Jeanmonod D (1997) Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 387:588–630

    Article  CAS  PubMed  Google Scholar 

  207. Battaglia G, Colacitti C, Bentivoglio M (1992) The relationship of calbindin-containing neurons with substance P, leu-enkephalin and cholecystokinin fibres: an immunohistochemical study in the rat thalamus. J Chem Neuroanat 5:453–464

    Article  CAS  PubMed  Google Scholar 

  208. Żakowski W, Bogus-Nowakowska K, Robak A (2013) Embryonic and postnatal development of calcium-binding proteins immunoreactivity in the anterior thalamus of the guinea pig. J Chem Neuroanat 53:25–32

    Article  PubMed  CAS  Google Scholar 

  209. Noonan D (1994) The guinea pig (Cavia porcellus). ANZCCART News 7:1–8

    Google Scholar 

  210. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613–622

    Article  CAS  PubMed  Google Scholar 

  211. Schanne FA, Kane AB, Young EE, Farber JL (1979) Calcium dependence of toxic cell death: a final common pathway. Science 206:700–702

    Article  CAS  PubMed  Google Scholar 

  212. Byatt G, Dalrymple-Alford JC (1996) Both anteromedial and anteroventral thalamic lesions impair radial-maze learning in rats. Behav Neurosci 110:1335–1348

    Article  CAS  PubMed  Google Scholar 

  213. Palczewska M, Groves P, Batta G, Heize B, Kuźnicki J (2003) Calretinin and calbindin D28k have different domain organization. Protein Sci 12:180–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475

    Article  CAS  PubMed  Google Scholar 

  215. Séquier JM, Hunziker W, Andressen C, Celio MR (1990) Calbindin D-28k protein and mRNA localization in the rat brain. Eur J Neurosci 2:1118–1126

    Article  PubMed  Google Scholar 

  216. Frassoni C, Bentivoglio M, Spreafico R, Sánchez MP, Puelles L, Fairen A (1991) Postnatal development of calbindin and parvalbumin immunoreactivity in the thalamus of the rat. Brain Res Dev Brain Res 58:243–249

    Article  CAS  PubMed  Google Scholar 

  217. Rogers JH, Résibois A (1992) Calretinin and calbindin-D28k in rat brain: patterns of partial co-localization. Neuroscience 51:843–865

    Article  CAS  PubMed  Google Scholar 

  218. Coveñas R, De León M, Narváez JA, Aguirre JA, González-Barón S (1995) Calbindin D-28K-immunoreactivity in the cat diencephalon: an immunocytochemical study. Arch Ital Biol 133:263–272

    PubMed  Google Scholar 

  219. Coveñas R, De León M, Alonso JR, Arévalo R, Lara J, Aijón J (1991) Distribution of parvalbumin-immunoreactivity in the rat thalamus using a monoclonal antibody. Arch Ital Biol 129:199–210

    PubMed  Google Scholar 

  220. De León M, Aguirre JA, Coveñas R, Narváez JA, González-Barón S (1995) Distribution of parvalbumin immunoreactivity in the cat diencephalon. Brain Res Bull 36:393–398

    Article  PubMed  Google Scholar 

  221. Dixon G, Dissanaike S, Harper CG (2000) Parvalbumin-immunoreactive neurons in the human anteroventral thalamic nucleus. Neuroreport 11:97–101

    Article  CAS  PubMed  Google Scholar 

  222. Douglass J, McKinzie AA, Couceyro P (1995) PCR differential display identifies a rat brain mRNA that is transcriptionally regulated by cocaine and amphetamine. J Neurosci 15:2471–2481

    CAS  PubMed  Google Scholar 

  223. Rogge G, Jones D, Hubert GW, Lin Y, Kuhar MJ (2008) CART peptides: regulators of body weight, reward and other functions. Nat Rev Neurosci 9:747–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Dun SL, Castellino SJ, Yang J, Chang JK, Dun NJ (2001) Cocaine- and amphetamine-regulated transcript peptide immunoreactivity in dorsal motor nucleus of the vagus neurons of immature rats. Brain Res Dev Brain Res 131:93–102

    Article  CAS  PubMed  Google Scholar 

  225. Brischoux F, Griffond B, Fellmann D, Risold PY (2002) Early and transient ontogenetic expression of the cocaine- and amphetamine-regulated transcript peptide in the rat mesencephalon: correlation with tyrosine hydroxylase expression. J Neurobiol 52:221–229

    Article  CAS  PubMed  Google Scholar 

  226. Risold PY, Bernard-Franchi G, Collard C, Jacquemard C, La Roche A, Griffond B (2006) Ontogenetic expression of CART-peptides in the central nervous system and the periphery: a possible neurotrophic role? Peptides 27:1938–1941

    Article  CAS  PubMed  Google Scholar 

  227. Bharne AP, Upadhya MA, Shelkar GP, Singru PS, Subhedar NK, Kokare DM (2012) Neuroprotective effect of cocaine- and amphetamine-regulated transcript peptide in spinal cord injury in mice. Neuropharmacology 67:126–135

    Article  PubMed  CAS  Google Scholar 

  228. Upadhya MA, Nakhate KT, Kokare DM, Singru PS, Subhedar NK (2011) Cocaine- and amphetamine-regulated transcript peptide increases spatial learning and memory in rats. Life Sci 88:322–334

    Article  CAS  PubMed  Google Scholar 

  229. Yermolaieva O, Chen J, Couceyro PR, Hoshi T (2001) Cocaine- and amphetamine-regulated transcript peptide modulation of voltage gated Ca2+ signaling in hippocampal neurons. J Neurosci 21:7474–7480

    CAS  PubMed  Google Scholar 

  230. Koylu EO, Couceyro PR, Lambert PD, Kuhar MJ (1998) Cocaine- and amphetamine-regulated transcript peptide immunohistochemical localization in the rat brain. J Comp Neurol 391:115–132

    Article  CAS  PubMed  Google Scholar 

  231. Żakowski W, Równiak M, Robak A (2014) Colocalization pattern of calbindin and cocaine- and amphetamine-regulated transcript in the mammillary body-anterior thalamic nuclei axis of the guinea pig. Neuroscience 260:98–105

    Article  PubMed  CAS  Google Scholar 

  232. Hunter RG, Lim MM, Philpot KB, Young LJ, Kuhar MJ (2005) Species differences in brain distribution of CART mRNA and CART peptide between prairie and meadow voles. Brain Res 1048:12–23

    Article  CAS  PubMed  Google Scholar 

  233. Hurd YL, Fagergren P (2000) Human cocaine- and amphetamine-regulated transcript (CART) mRNA is highly expressed in limbic- and sensory-related brain regions. J Comp Neurol 425:583–598

    Article  CAS  PubMed  Google Scholar 

  234. Khachaturian H, Lewis EJ, Schafer MK, Watson SJ (1985) Anatomy of the CNS opioid systems. Trends Neurosci 3:111–119

    Article  Google Scholar 

  235. Coveñas R, Alonso JR, Conrath M (1989) Immunocytochemical study of enkephalin-like cell bodies in the thalamus of the rat. Brain Res Bull 23:277–281

    Article  PubMed  Google Scholar 

  236. Fujii S, Senba E, Kiyama H, Ueda Y, Tohyama M (1987) Mammillothalamic enkephalinergic pathway in the rat: an immunocytochemical analysis. Brain Res 401:1–8

    Article  CAS  PubMed  Google Scholar 

  237. Coveñas R, Romo R, Cheramy A, Cesselin F, Conrath M (1986) Immunocytochemical study of enkephalin-like cell bodies in the thalamus of the cat. Brain Res 377:355–361

    Article  PubMed  Google Scholar 

  238. Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V (2002) The tachykinin peptide family. Pharmacol Rev 54:285–322

    Article  CAS  PubMed  Google Scholar 

  239. Burgos C, Aguirre JA, Alonso JR, Coveñas R (1988) Immunocytochemical study of substance P-like fibres and cell bodies in the cat diencephalon. J Hirnforsch 29:651–657

    CAS  PubMed  Google Scholar 

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Acknowledgments

This study was funded by National Science Centre in Poland (postdoctoral internship program FUGA 3, grant no. DEC-2014/12/S/NZ3/00621) and by the Faculty of Biology, University of Gdańsk, Poland. The author would like to thank Magda Kuśmierczak Ph.D. for linguistic revision.

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Correspondence to Witold Żakowski.

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Żakowski, W. Neurochemistry of the Anterior Thalamic Nuclei. Mol Neurobiol 54, 5248–5263 (2017). https://doi.org/10.1007/s12035-016-0077-y

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  • DOI: https://doi.org/10.1007/s12035-016-0077-y

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