Paraventricular thalamic nucleus: Subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in Macaque monkeys

Journal of Comparative Neurology

Volumn 512, Issue 6, 2009, Pages 825-848

  Hsu, David T ^a   Price, Joseph L ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Accumbens nucleus; Amygdala; Caudate nucleus; Depression; Hypothalamus; Mood disorders; Paratenial nucleus; Periaqueductal gray; Stress; Striatum

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; OREXIN; SEROTONIN; TRACER; NEUROPEPTIDE; OREXINS; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INNERVATION; MACACA; MESENCEPHALON; MONKEY; NERVE FIBER; NONHUMAN; NUCLEUS ACCUMBENS; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; STRESS; THALAMUS MIDLINE NUCLEUS; ANIMAL; HISTOLOGY; HUMAN; METABOLISM; NERVE TRACT;

ANIMALS; CORTICOTROPIN-RELEASING HORMONE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACACA FASCICULARIS; MIDLINE THALAMIC NUCLEI; NEURAL PATHWAYS; NEUROPEPTIDES; SEROTONIN;

EID: 59649097112     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21934     Document Type: Article

References (127)

1. Abrams JK, Johnson PL, Hollis JH, Lowry CA. 2004. Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 1018:46-57.
2. Aggleton JP, Burton MJ, Passingham RE. 1980. Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 190:347-368.
3. Aggleton JP, Desimone R, Mishkin M. 1986. The origin, course, and termination of the hippocampothalamic projections in the macaque. 243:409-421.
4. Amaral DG, Price JL. 1984. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465-496.
5. An X, Bandler R, _Odsngür D, Price JL. 1998. Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 401:455-479.
6. Angeles-Castellanos M, Mendoza J, Escobar C. 2007. Restricted feeding schedules phase shift daily rhythms of c-Fos and protein Per1 immunoreactivity in corticolimbic regions in rats. Neuroscience 144:344-355.
7. Arango V, Underwood MD, Mann JJ. 2002. Serotonin brain circuits involved in major depression and suicide. Prog Brain Res 136:443-453.
8. Arbelaez AM, Powers WJ, Videen TO, Price JL, Cryer PE. 2007. Attenuation of counterregulatory responses to recurrent hypoglycemia by active thalamic inhibition: a mechanism for hypoglycemia-associated autonomic failure. Diabetes 57:470-455.
9. Baldo BA, Daniel RA, Berridge CW, Kelley AE. 2003. Overlapping distributions of orexin/hypocretin- and dopamine-beta-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J Comp Neurol 464:220-237.
10. Bassett JL, Foote SL. 1992. Distribution of corticotropin-releasing factor-like immunoreactivity in squirrel monkey (Saimiri sciureus) amygdala. J Comp Neurol 323:91-102.
11. Beck CH, Fibiger HC. 1995. Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J Neurosci 15:709-720.
12. Beckstead RM. 1984. The thalamostriatal projection in the cat. J Comp Neurol 223:313-346.
13. Berendse HW, Groenewegen HJ. 1990. Organization of the thalaostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299:187-228.
14. Berendse HW, Groenewegen HJ. 1991. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:73-102.
15. Bhatnagar S, Dallman M. 1998. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84:1025-1039.
16. Bhatnagar S, Huber R, Nowak N, Trotter P. 2002. Lesions of the posterior paraventricular thalamus block habituation of hypothalamic-pituitary-adrenal responses to repeated restraint. J Neuroendocrinol 14:403-410.
17. Bhatnagar S, Huber R, Lazar E, Pych L, Vining C. 2003. Chronic stress alters behavior in the conditioned defensive burying test: role of the posterior paraventricular thalamus. Pharmacol Biochem Behav 76: 343-349.
18. Boutrel B, Kenny PJ, Specio SE, Martin-Fardon R, Markou A, Koob GF, de Lecea L. 2005. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci U S A 102:19168-19173.
19. Brady KT, Sinha R. 2005. Co-occurring mental and substance use disorders: the neurobiological effects of chronic stress. Am J Psychiatry 162:1483-1493.
20. Brauer K, Häusser M, Härtig W, Arendt T. 2000. The core-shell dichotomy of nucleus accumbens in the rhesus monkey as revealed by double-immunofluorescence and morphology of cholinergic interneurons. Brain Res 858:151-162.
21. Breiter HC, Rosen BR. 1999. Functional magnetic resonance imaging of brain reward circuitry in the human. Ann N Y Acad Sci 877:523-547.
22. Brody AL, Saxena S, Mandelkern MA, Fairbanks LA, Ho ML, Baxter LR. 2001. Brain metabolic changes associated with symptom factor improvement in major depressive disorder. Biol Psychiatry 50:171-178.
23. Bubser M, Deutch AY. 1999. Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites. Synapse 32:13-22.
24. Carmichael ST, Price JL. 1994. Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366-402.
25. Carmichael ST, Price JL. 1995. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363: 615-641.
26. Cha CI, Foote SL. 1988. Corticotropin-releasing factor in olivocerebellar climbing-fiber system of monkey (Saimiri sciureus and Macaca fascicularis): parasagittal and regional organization visualized by immunohistochemistry. J Neurosci 8:4121-4137.
27. Chastrette N, Pfaff DW, Gibbs RB. 1991. Effects of daytime and nighttime stress on Fos-like immunoreactivity in Paraventricular nucleus of the hypothalamus, the habenula, and the posterior paraventricular nucleus of the thalamus. Brain Res 563:339-344.
28. Chen S, Su HS. 1990. Afferent connections of the thalamic paraventricular and paratenial nuclei in the rat-a retrograde tracing study with iontophoretic application of Fluoro-Gold. Brain Res 522:1-6.
29. Commons KG, Connolley KR, Valentino RJ. 2003. A neurochemically distinct dorsal raphe-limbic circuit with a potential role in affective disorders. Neuropsychopharmacology 28:206-215.
30. Cornwall J, Phillipson OT. 1988. Afferent projections to the dorsal thalamus of the rat as shown by retrograde lectin transport. II. The midline nuclei. Brain Res Bull 21:147-161.
31. Crocker A, España RA, Papadopoulou M, Saper CB, Faraco J, Sakurai T, Honda M, Mignot E, Scammell TE. 2005. Concomitant loss of dynorphin, NARP, and orexin in narcolepsy. Neurology 65:1184-1188.
32. Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ. 1995. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477-505.
33. Deadwyler SA, Hayashizaki S, Cheer J, Hampson RE. 2004. Reward, memory and substance abuse: functional neuronal circuits in the nucleus accumbens. Neurosci Biobehav Rev 27:703-711.
34. Drevets WC. 1999. Prefrontal cortical-amygdalar metabolism in major depression. Ann N Y Acad Sci. 877:614-637.
35. Drevets WC, Price JL, Simpson JR Jr, Todd RD, Reich T, Vannier M, Raichle ME. 1997. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824-827.
36. Duncan GE, Johnson KB, Breese GR. 1993. Topographic patterns of brain activity in response to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity. J Neurosci 13: 3932-3943.
37. Epstein J, Pan H, Kocsis JH, Yang Y, Butler T, Chusid J, Hochberg H, Murrough J, Strohmayer E, Stern E, Silbersweig DA. 2006. Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. Am J Psychiatry 163:1784-1790.
38. Ferry AT, Öngür D, An X, Price JL. 2000. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol 425:447-470.
39. Foote SL, Cha CI. 1988. Distribution of corticotropin-releasing-factor-like immunoreactivity in brainstem of two monkey species (Saimiri sciureus and Macaca fascicularis): an immunohistochemical study. J Comp Neurol 276:239-264.
40. Freedman LJ, Cassell MD. 1994. Relationship of thalamic basal forebrain projection neurons to the peptidergic innervation of the midline thalamus. J Comp Neurol 348:321-342.
41. Gardner KL, Thrivikraman KV, Lightman SL, Plotsky PM, Lowry CA. 2005. Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 136:181-191.
42. Giménez-Amaya JM, McFarland NR, de las Heras S, Haber SN. 1995. Organization of thalamic projections to the ventral striatum in the primate. J Comp Neurol 354:127-149.
43. Grahn RE, Maswood S, McQueen MB, Watkins LR, Maier SF. 1999. Opioid-dependent effects of inescapable shock on escape behavior and conditioned fear responding are mediated by the dorsal raphe nucleus. Behav Brain Res 99:153-167.
44. Gray TS, Morley JE. 1986. Neuropeptide Y: anatomical distribution and possible function in mammalian nervous system. Life Sci 38:389-401.
45. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, Kenna H, Reiss AL, Schatzberg AF. 2007. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62:429-437.
46. Hammack SE, Richey KJ, Schmid MJ, LoPresti ML, Watkins LR, Maier SF. 2002. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J Neurosci 22:1020-1026.
47. Harris GC, Wimmer M, Aston-Jones G. 2005. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556-559.
48. Hasler G, Drevets WC, Manji HK, Charney DS. 2004. Discovering endophenotypes for major depression. Neuropsychopharmacology 29: 1765-1781.
49. Horvath TL, Diano S, van den Pol AN. 1999. Synaptic interaction between hypocretin (orexin) and neuropeptide Y cells in the rodent and primate hypothalamus: a novel circuit implicated in metabolic and endocrine regulations. J Neurosci 19:1072-1087.
50. Hsu DT, Price JL. 2007. Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol 504:89-111.
51. Imai H, Steindler DA, Kitai ST. 1986. The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 243:363-380.
52. Imaki T, Shibasaki T, Hotta M, Demura H. 1993. Intracerebroventricular administration of corticotropin-releasing factor induces c-fos mRNA expression in brain regions related to stress responses: comparison with pattern of c-fos mRNA induction after stress. Brain Res 616:114-125.
53. Insausti R, Amaral DG, Cowan WM. 1987. The entorhinal cortex of the monkey: III. Subcortical afferents. J Comp Neurol 264:396-408.
54. Ishibashi M, Takano S, Yanagida H, Takatsuna M, Nakajima K, Oomura Y, Wayner MJ, Sasaki K. 2005. Effects of orexins/hypocretins on neuronal activity in Paraventricular nucleus of the thalamus in rats in vitro. Peptides 26:471-481.
55. Jaferi A, Nowak N, Bhatnagar S. 2003. Negative feedback functions in chronically stressed rats: role of the posterior paraventricular thalamus. Physiol Behav 78:365-373.
56. Jones EG. 2007. The thalamus, 2nd ed. New York: Cambridge University Press.
57. Jones EG, Leavitt RY. 1974. Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J Comp Neurol 154:349-378.
58. Kelley AE, Baldo BA, Pratt WE. 2005. A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol 493:72-85.
59. Kirouac GJ, Parsons MP, Li S. 2005. Orexin (hypocretin) innervation of paraventricular nucleus of the thalamus. Brain Res 1059:179-188.
60. Kritzer MF, Goldman-Rakic PS. 1995. Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey. J Comp Neurol 359:131-143.
61. Krout KE, Loewy. 2000a. Parabrachial nucleus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 428:475-494.
62. Krout KE, Loewy. 2000b. Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 424:111-141.
63. LaMotte CC. 1988. Lamina X of primate spinal cord: distribution of five neuropeptides and serotonin. Neuroscience 25:639-658.
64. Landry GJ, Yamakawa GR, Mistlberger RE. 2007. Robust food anticipatory circadian rhythms in rats with complete ablation of the thalamic paraventricular nucleus. Brain Res 1141:108-118.
65. Langevin H, Emson PC. 1982. Distribution of substance P, somatostatin and neurotensin in the human hypothalamus. Brain Res 246:65-69.
66. Larsen PJ. 1992. Distribution of substance P-immunoreactive elements in the preoptic area and the hypothalamus of the rat. J Comp Neurol 316:287-313.
67. Lavoie B, Parent A. 1991. Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J Comp Neurol 312:1-18.
68. Li S, Kirouac GJ. 2008. Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 506:263-287.
69. Maier SF, Watkins LR. 2005. Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29:829-841.
70. Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA, Silva JA, Tekell JL, Martin CC, Lancaster JL, Fox PT. 1999. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 156:675-682.
71. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, Schwalb JM, Kennedy SH. 2005. Deep brain stimulation for treatment-resistant depression. Neuron 45:651-660.
72. McKenna JT, Vertes RP. 2004. Afferent projections to nucleus reuniens of the thalamus. J Comp Neurol 480:115-142.
73. Mehler WR. 1980. Subcortical afferent connections of the amygdala in the monkey. J Comp Neurol 190:733-762.
74. Meloni EG, Reedy CL, Cohen BM, Carlezon WA Jr. 2008. Activation of raphe efferents to the medial prefrontal cortex by corticotropin-releasing factor: correlation with anxiety-like behavior. Biol Psychiatry 63:832-839.
75. Meredith GE, Pattiselanno A, Groenewegen HJ, Haber SN. 1996. Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin-D28k. J Comp Neurol 365:628-639.
76. Moga MM, Weis RP, Moore RY. 1995. Efferent projections of Paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221-238.
77. Moore RY, Speh JC. 2004. Serotonin innervation of the primate suprachiasmatic nucleus. Brain Res 1010:169-173.
78. Nakahara K, Fukui K, Murakami N. 2004. Involvement of thalamic paraventricular nucleus in the anticipatory reaction under food restriction in the rat. J Vet Med Sci 66:1297-1300.
79. Nambu T, Sakurai T, Mizukami K, Hosoya Y, Yanagisawa M, Goto K. 1999. Distribution of orexin neurons in the adult rat brain. Brain Res 827: 243-260.
80. Nemeroff CB. 1988. The role of corticotropin-releasing factor in Pathogenesis of major depression. Pharmacopsychiatry 21:76-82.
81. Novak CM, Nunez AA. 1998. Daily rhythms in Fos activity in the rat ventrolateral preoptic area and midline thalamic nuclei. Am J Physiol 275:R1620-1626.
82. Oldfield BJ, Silverman AJ. 1985. A light microscopic HRP study of limbic projections to the vasopressin-containing nuclear groups of the hypothalamus. Brain Res Bull 14:143-157.
83. Olszewski J. 1952. The thalamus of the Macaca mulatta. An atlas for use with the stereotaxic instrument. New York: Karger.
84. Öngür D, Price JL. 2000. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206-219.
85. Öngür D, An X, Price JL. 1998. Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 401:480-505.
86. Otake K. 2005. Cholecystokinin and substance P immunoreactive projections to the paraventricular thalamic nucleus in the rat. Neurosci Res 51:383-394.
87. Otake K, Nakamura Y. 1995. Sites of origin of corticotropin-releasing factor-like immunoreactive projection fibers to Paraventricular thalamic nucleus in the rat. Neurosci Lett 201:84-86.
88. Otake K, Kin K, Nakamura Y. 2002. Fos expression in afferents to the rat midline thalamus following immobilization stress. Neurosci Res 43: 269-282.
89. Périco CA, Skaf CR, Yamada A, Duran F, Buchpiguel CA, Castro CC, Soares JC, Busatto GF. 2005. Relationship between regional cerebral blood flow and separate symptom clusters of major depression: a single photon emission computed tomography study using statistical parametric mapping. Neurosci Lett 384:265-270.
90. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS. 1998. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015.
91. Pierce TL, Wessendorf MW. 2000. Immunocytochemical mapping of endomorphin-2-immunoreactivity in rat brain. J Chem Neuroanat 18: 181-207.
92. Pizzagalli DA, Oakes TR, Fox AS, Chung MK, Larson CL, Abercrombie HC, Schaefer SM, Benca RM, Davidson RJ. 2004. Functional but not structural subgenual prefrontal cortex abnormalities in melancholia. Mol Psychiatry 9:393-405.
93. Price JL. 2003. Comparative aspects of amygdala connectivity. Ann N Y Acad Sci 985:50-58.
94. Price JL. 2007. Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54-71.
95. Price JL, Amaral DG. 1981. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242-1259.
96. Royce GJ, Bromley S, Gracco C, Beckstead RM. 1989. Thalamocortical connections of the rostral intralaminar nuclei: an autoradiographic analysis in the cat. J Comp Neurol 288:555-582.
97. Sakurai T. 2007. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8:171-181.
98. Salazar-Juárez A, Escobar C, Aguilar-Roblero R. 2002. Anterior paraventricular thalamus modulates light-induced phase shifts in circadian rhythmicity in rats. Am J Physiol Regul Integr Comp Physiol 283:R897-904.
99. Sánchez-González MÁ, García-Cabezas MÁ, Rico B, Cavada C. 2005. The primate thalamus is a key target for brain dopamine. J Neurosci 25:6076-6083.
100. Saper CB, Scammell TE, Lu J. 2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257-1263.
101. Saunders RC, Mishkin M, Aggleton JP. 2005. Projections from the entorhinal cortex, perirhinal cortex, presubiculum, and parasubiculum to the medial thalamus in macaque monkeys: identifying different pathways using disconnection techniques. Exp Brain Res 167:1-16.
102. Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N, Joe AY, Kreft M, Lenartz D, Sturm V. 2008. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33:368-377.
103. Semba K, Pastorius J, Wilkinson M, Rusak B. 2001. Sleep deprivation-induced c-fos and junB expression in the rat brain: effects of duration and timing. Behav Brain Res 120:75-86.
104. Senba E, Matsunaga K, Tohyama M, Noguchi K. 1993. Stress-induced c-fos expression in the rat brain: activation mechanism of sympathetic pathway. Brain Res Bull 31:329-344.
105. Sharp FR, Sagar SM, Hicks K, Lowenstein D, Hisanaga K. 1991. c-fos mRNA, Fos, and Fos-related antigen induction by hypertonic saline and stress. J Neurosci 11:2321-2331.
106. Shekhtman E, Geerling JC, Loewy AD. 2007. Aldosterone-sensitive neurons of the nucleus of the solitary tract: multisynaptic pathway to the nucleus accumbens. J Comp Neurol. 501:274-289.
107. Sica AL, Greenberg HE, Scharf SM, Ruggiero DA. 2000. Chronic-intermittent hypoxia induces immediate early gene expression in the midline thalamus and epithalamus. Brain Res 883:224-228.
108. Siegle GJ, Carter CS, Thase ME. 2006. Use of fMRI to predict recovery from unipolar depression with cognitive behavior therapy. Am J Psychiatry 163:735-738.
109. Silverman AJ, Oldfield BJ. 1984. Synaptic input to vasopressin neurons of paraventricular nucleus (PVN). Peptides 5(Suppl 1):139-150.
110. Spencer SJ, Fox JC, Day TA. 2004. Thalamic paraventricular nucleus lesions facilitate central amygdala neuronal responses to acute psychological stress. Brain Res 997:234-237.
111. Su HS, Bentivoglio M. 1990. Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J Comp Neurol 297:582-593.
112. Sutcliffe JG, de Lecea L. 2000. The hypocretins: excitatory neuromodulatory peptides for multiple homeostatic systems, including sleep and feeding. J Neurosci Res 62:161-168.
113. Swanson LW, Sawchenko PE, Rivier J, Vale WW. 1983. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165-186.
114. Szabo J, Cowan WM. 1984. A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 222:265-300.
115. Teves D, Videen TO, Cryer PE, Powers WJ. 2004. Activation of human medial prefrontal cortex during autonomic responses to hypoglycemia. Proc Natl Acad Sci U S A 101:6217-6221.
116. Uroz V, Prensa L, Giménez-Amaya JM. 2004. Chemical anatomy of the human paraventricular thalamic nucleus. Synapse 51:173-185.
117. Van der Werf YD, Witter MP, Groenewegen HJ. 2002. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39:107-140.
118. Van Laere K, Nuttin B, Gabriels L, Dupont P, Rasmussen S, Greenberg BD, Cosyns P. 2006. Metabolic imaging of anterior capsular stimulation in refractory obsessive-compulsive disorder: a key role for the subgenual anterior cingulate and ventral striatum. J Nucl Med 47:740-747.
119. Vertes RP. 1991. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643-668.
120. Vertes RP, Hoover WB. 2008. Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212-237.
121. Vertes RP, Fortin WJ, Crane AM. 1999. Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555-582.
122. Vogt BA, Hof PR, Friedman DP, Sikes RW, Vogt LJ. 2008. Norepinephrinic afferents and cytology of the macaque monkey midline, mediodorsal, and intralaminar thalamic nuclei. Brain Struct Funct 212:465-480.
123. Watts AG, Swanson LW. 1987. Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 258:230-252.
124. Watts AG, Swanson LW, Sanchez-Watts G. 1987. Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol 258:204-229.
125. Westlund KN, Sorkin LS, Ferrington DG, Carlton SM, Willcockson HH, Willis WD. 1990. Serotoninergic and noradrenergic projections to the ventral posterolateral nucleus of the monkey thalamus. J Comp Neurol 295:197-207.
126. Yanagihara M, Niimi K, Ono K. 1987. Thalamic projections to the hippocampal and entorhinal areas in the cat. J Comp Neurol 266:122-141.
127. Zhang DX, Bertram EH. 2002. Midline thalamic region: widespread excitatory input to the entorhinal cortex and amygdala. J Neurosci 15: 3277-3284.