Amygdala projections to the lateral bed nucleus of the stria terminalis in the macaque: Comparison with ventral striatal afferents

Journal of Comparative Neurology

Volumn 521, Issue 14, 2013, Pages 3191-3216

  deCampo, Danielle M ^a   Fudge, Julie L ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Amygdalopiriform transition area; Anxiety; Corticoamygdaloid transition region; Dorsomedial shell; Extended amygdala; Juxtacapsular; Oval

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR AMYGDALOID AREA; ARTICLE; BASAL AMYGDALA; BASAL NUCLEUS MAGNOCELLULAR SUBDIVISION; BASAL NUCLEUS PARVICELLULAR SUBDIVISION; CAUDATE NUCLEUS; CELL LABELING; CELLULAR DISTRIBUTION; CENTRAL NUCLEUS LATERAL SUBDIVISION; CENTRAL NUCLEUS MEDIAL SUBDIVISION; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOAMYGDALOID TRANSITION AREA; DORSOMEDIAL SHELL; MACACA FASCICULARIS; MACACA NEMESTRINA; MALE; MEDIAL NUCLEUS; MEDULLA OBLONGATA LATERAL NUCLEUS; NEUROANATOMICAL TRACT TRACING; NONHUMAN; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; SENSORY NERVE; STIMULUS RESPONSE; STRIA TERMINALIS; STRIA TERMINALIS LATERAL BED NUCLEUS CENTRAL SUBDIVISION; STRIA TERMINALIS LATERAL BED NUCLEUS JUXTACAPSULAR SUBDIVISION; STRIA TERMINALIS LATERAL BED NUCLEUS ROSTRALMOST SUBDIVISION; SUBCORTEX; VENTRAL SHELL;

AMYGDALOPIRIFORM TRANSITION AREA; ANXIETY; CORTICOAMYGDALOID TRANSITION REGION; DORSOMEDIAL SHELL; EXTENDED AMYGDALA; JUXTACAPSULAR; OVAL;

AFFERENT PATHWAYS; AMYGDALA; ANIMALS; AUTORADIOGRAPHY; CALBINDIN 1; CHOLINESTERASES; CORPUS STRIATUM; ENKEPHALIN, METHIONINE; FUNCTIONAL LATERALITY; ISOQUINOLINES; MACACA NEMESTRINA; MALE; NEUROTENSIN; SEPTAL NUCLEI; SOMATOSTATIN; WHEAT GERM AGGLUTININ-HORSERADISH PEROXIDASE CONJUGATE;

EID: 84881257736     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23340     Document Type: Article

References (104)

1. Aggleton JP, Mishkin M. 1984. Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56-68.
2. Aggleton JP, Friedman DP, Mishkin M. 1987. A comparison between the connections of the amygdala and hippocampus with the basal forebrain in the macaque. Exp Brain Res 67:556-568.
3. Alheid GF, Heimer L. 1988. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1-39.
4. Alheid GF, DeOlmos CA, Beltramino CA. 1995. Amygdala and extended amygdala. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press. p 495-578.
5. Alvarez RP, Chen G, Bodurka J, Kaplan R, Grillon C. 2011. Phasic and sustained fear in humans elicits distinct patterns of brain activity. Neuroimage 55:389-400.
6. Amaral DG, Bassett JL. 1989. Cholinergic innervation of the monkey amygdala: an immunohistochemical analysis with antisera to choline acetyltransferase. J Comp Neurol 281:337-361.
7. Amaral DG, Price JL, Pitkanen A, Carmichael ST. 1992. Anatomical organization of the primate amygdaloid complex. The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss. p 1-66.
8. Brog JS, Salyapongse A, Deutch AY, Zahm DS. 1993. The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338:255-278.
9. Canteras NS, Swanson LW. 1992. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324:180-194.
10. Canteras NS, Simerly RB, Swanson LW. 1992. Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143-179 [erratum, J Comp Neurol 1993;22;328:604].
11. Carmichael ST, Price JL. 1996. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615-641.
12. Carmichael ST, Clugnet MC, Price JL. 1994. Central olfactory connections in the macaque monkey. J Comp Neurol 346:403-434.
13. Chang HT, Kuo H. 1991. Relationship of calbindin D-28k and cholinergic neurons in the nucleus basalis of Meynert of the monkey and the rat. Brain Res 549:141-145.
14. Cote P-Y, Sadikot AF, Parent A. 1991. Complementary distribution of calbindin D-28k and parvalbumin in the basal forebrain and midbrain of the squirrel monkey. Eur J Neurosci 3:1316-1329.
15. Craig AD. 2002. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655-666.
16. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. 2004. Neural systems supporting interoceptive awareness. Nat Neurosci 7:189-195.
17. Crosby EC, Humphrey T. 1941. Studies of the vertebrate telencephalon: the nuclear pattern of the anterior olfactory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man. J Comp Neurol 74:309-347.
18. De Olmos JS. 1990. Amygdala. In: Paxinos G, editor. The human nervous system. San Diego: Academic Press. p 583-710.
19. De Olmos J. 2004. The amygdala. In: Paxinos G, Mai JK, editors. The human nervous system, 2nd ed. San Diego: Elsevier Academic Press.
20. deCampo DM, Fudge JL. 2012. Where and what is the paralaminar nucleus? A review on a unique and frequently overlooked area of the primate amygdala. Neurosci Biobehav Rev 36:520-535.
21. Dong H, Petrovich GD, Swanson LW. 2000. Organization of projections from the juxtacapsular nucleus of the BST: a PHAL study in the rat. Brain Res 859:1-14.
22. Dong HW, Petrovich GD, Swanson LW. 2001a. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38:192-246.
23. Dong HW, Petrovich GD, Watts AG, Swanson LW. 2001b. Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J Comp Neurol 436:430-455.
24. Duvarci S, Bauer EP, Pare D. 2009. The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J Neurosci 29:10357-10361.
25. Fendt M, Endres T, Apfelbach R. 2003. Temporary inactivation of the bed nucleus of the stria terminalis but not of the amygdala blocks freezing induced by trimethylthiazoline, a component of fox feces. J Neurosci 23:23-28.
26. Fox AS, Shelton SE, Oakes TR, Davidson RJ, Kalin NH. 2008. Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS One 3:e2570.
27. Francesconi W, Berton F, Repunte-Canonigo V, Hagihara K, Thurbon D, Lekic D, Specio SE, Greenwell TN, Chen SA, Rice KC, Richardson HN, O'Dell LE, Zorrilla EP, Morales M, Koob GF, Sanna PP. 2009. Protracted withdrawal from alcohol and drugs of abuse impairs long-term potentiation of intrinsic excitability in the juxtacapsular bed nucleus of the stria terminalis. J Neurosci 29:5389-5401.
28. Freedman LJ, Insel TR, Smith Y. 2000. Subcortical projections of area 25 (subgenual cortex) of the macaque monkey. J Comp Neurol 421:172-188.
29. Friedman DP, Aggleton JP, Saunders RC. 2002. Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: combined anterograde and retrograde tracing study in the Macaque brain. J Comp Neurol 450:345-365.
30. Fudge JL, Haber SN. 2001. Bed nucleus of the stria terminalis and extended amygdala inputs to dopamine subpopulations in primates. Neuroscience 104:807-827.
31. Fudge JL, Tucker T. 2009. Amygdala projections to central amygdaloid nucleus subdivisions and transition zones in the primate. Neuroscience 159:819-841.
32. Fudge JL, Kunishio K, Walsh P, Richard C, Haber SN. 2002. Amygdaloid projections to ventromedial striatal subterritories in the primate. Neuroscience 110:257-275.
33. Fudge JL, Breitbart MA, McClain C. 2004. Amygdaloid inputs define a caudal component of the ventral striatum in primates. J Comp Neurol 476:330-347.
34. Fudge JL, deCampo DM, Becoats KT. 2012. Revisiting the hippocampal-amygdala pathway in primates: association with immature-appearing neurons. Neuroscience 212:104-119.
35. Geneser-Jensen FA, Blackstad TW. 1971. Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. Z Zellforsch 114:460-481.
36. Ghashghaei HT, Barbas H. 2001. Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey. Neuroscience 103:593-614.
37. Gracy KN, Dankiewicz LA, Koob GF. 2001. Opiate withdrawal-induced fos immunoreactivity in the rat extended amygdala parallels the development of conditioned place aversion. Neuropsychopharmacology 24:152-160.
38. Grove EA. 1988. Neural associations of the substantia innominata in the rat: afferent connections. J Comp Neurol 277:315-346.
39. Haber SN, Fudge JL, McFarland N. 2000. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20:2369-2382.
40. Halperin JJ, LaVail JH. 1975. A study of the dynamics of retrograde transport and accumulation of horseradish peroxidase in injured neurons. Brain Res 100:253-269.
41. Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE, Zahm DS. 1997. The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci 9:354-381.
42. Heimer L, De Olmos JS, Alheid GF, Person J, Sakamoto N, Shinoda K, Marksteiner J, Switzer RC. 1999. The human basal forebrain. Part II. In: Bloom FE, Bjorkland A, Hokfelt T, editors. Handbook of chemical neuroanatomy. Amsterdam: Elsevier. p 57-226.
43. Hoistad M, Barbas H. 2008. Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala. Neuroimage 40:1016-1033.
44. Ikemoto S, Qin M, Liu ZH. 2005. The functional divide for primary reinforcement of D-amphetamine lies between the medial and lateral ventral striatum: is the division of the accumbens core, shell, and olfactory tubercle valid? J Neurosci 25:5061-5065.
45. Insausti R, Herrero MT, Witter MP. 1997. Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7:146-183.
46. Jolkkonen E, Miettinen R, Pitkanen A. 2001. Projections from the amygdalo-piriform transition area to the amygdaloid complex: a PHA-l study in rat. J Comp Neurol 432:440-465.
47. Ju G, Swanson LW, Simerly RB. 1989. Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat. II. Chemoarchitecture. J Comp Neurol 280:603-621.
48. Kelley AE. 1999. Functional specificity of ventral striatal compartments in appetitive behaviors. Ann N Y Acad Sci 877:71-90.
49. Koob GF, Volkow ND. 2010. Neurocircuitry of addiction. Neuropsychopharmacology 35:217-238.
50. Krettek JE, Price JL. 1977. Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat. J Comp Neurol 172:723-752.
51. Krettek JE, Price JL. 1978. Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225-254.
52. Lanciego JL, Wouterlood FG. 2011. A half century of experimental neuroanatomical tracing. J Chem Neuroanat 42:157-183.
53. Larriva-Sahd J. 2004. Juxtacapsular nucleus of the stria terminalis of the adult rat: extrinsic inputs, cell types, and neuronal modules: a combined Golgi and electron microscopic study. J Comp Neurol 475:220-237.
54. Lesur A, Gaspar P, Alvarez C, Berger B. 1989. Chemoanatomic compartments in the human bed nucleus of the stria terminalis. Neuroscience 321:181-194.
55. Mai JK, Triepel J, Metz J. 1987. Neurotensin in the human brain. Neuroscience 222:499-524.
56. Martin LJ, Powers RE, Dellovade TL, Price DL. 1991. The bed nucleus-amygdala continuum in human and monkey. J Comp Neurol 309:445-485.
57. McDonald AJ. 1983. Neurons of the bed nucleus of the stria terminalis: a Golgi study in the rat. Brain Res Bull 10:111-120.
58. McDonald AJ. 1991. Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 441:15-33.
59. McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257-332.
60. McDonald AJ, Shammah-Lagnado SJ, Shi C, Davis M. 1999. Cortical afferents to the extended amygdala. Ann N Y Acad Sci 877:309-338.
61. 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.
62. Miyashita T, Ichinohe N, Rockland KS. 2007. Differential modes of termination of amygdalothalamic and amygdalocortical projections in the monkey. J Comp Neurol 502:309-324.
63. Mobbs D, Yu R, Rowe JB, Eich H, FeldmanHall O, Dalgleish T. 2010. Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc Natl Acad Sci U S A 107:20582-20586.
64. Moga MM, Saper CB, Gray TS. 1989. Bed nucleus of the stria terminalis: cytoarchitecture, immunohistochemistry, and projection to the parabrachial nucleus in the rat. J Comp Neurol 283:315-332.
65. Mufson EJ, Mesulam MM, Pandya DN. 1981. Insular interconnections with the amygdala in the rhesus monkey. Neuroscience 6:1231-1248.
66. Nance DM, Burns J. 1990. Fluorescent dextrans as sensitive anterograde neuroanatomical tracers: applications and pitfalls. Brain Res Bull 25:139-145.
67. Naya Y, Suzuki WA. 2011. Integrating what and when across the primate medial temporal lobe. Science 333:773-776.
68. Novotny GEK. 1977. A direct ventral connection between the bed nucleus of the stria terminalis and the amygdaloid complex in the monkey (Macaca fascicularis). J Hirnforsch 18:271-284.
69. Ottersen OP, Ben-Ari Y. 1979. Afferent connections to the amygdaloid complex of the rat and cat. I. Projections from the thalamus. J Comp Neurol 187:401-424.
70. Paz R, Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I. 2010. A neural substrate in the human hippocampus for linking successive events. Proc Natl Acad Sci U S A 107:6046-6051.
71. Petrovich GD, Swanson LW. 1997. Projections from the lateral part of the central amygdalar nucleus to the postulated fear conditioning circuit. Brain Res 763:247-254.
72. Petrovich GD, Risold PY, Swanson LW. 1996. Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374:387-420.
73. Pitkanen A, Amaral DG. 1998. Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 398:431-458.
74. Porrino LJ, Crane AM, Goldman-Rakic PS. 1981. Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. J Comp Neurol 198:121-136.
75. Price JL, Amaral DG. 1981. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242-1259.
76. Price JL, Russchen FT, Amaral DG. 1987. The limbic region. II. The amygdaloid complex. In: Hokfelt BT, Swanson LW, editors. Handbook of chemical neuroanatomy. Amsterdam: Elsevier. p 279-381.
77. Reynolds SM, Berridge KC. 2002. Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste "liking"/"disliking" reactions, place preference/avoidance, and fear. J Neurosci 22:7308-7320.
78. Rosene DL, Van Hoesen GW. 1977. Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198:315-317.
79. Rosene D, Van Hoesen G. 1987. The hippocampal formation of the primate brain. In: Jones E, Peters A, editors. Cerebral cortex: further aspects of cortical function, including hippocampus. New York: Plenum Press. p 345-456.
80. Rosene DL, Roy NJ, Davis BJ. 1986. A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. J Histochem Cytochem 3410:1301-1315.
81. Russchen FT, Amaral DG, Price JL. 1985a. The afferent connections of the substantia innominata in the monkey, Macaca fascicularis. J Comp Neurol 242:1-27.
82. Russchen FT, Bakst I, Amaral DG, Price JL. 1985b. The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res 329:241-257.
83. Russchen FT, Amaral DG, Price JL. 1987. The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J Comp Neurol 256:175-210.
84. Santiago AC, Shammah-Lagnado SJ. 2005. Afferent connections of the amygdalopiriform transition area in the rat. J Comp Neurol 489:349-371.
85. Saunders RC, Rosene DL, Van Hoesen GW. 1988. Comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey. II. Reciprocal and non-reciprocal connections. J Comp Neurol 271:185-207.
86. Schmued L, Kyriakidis K, Heimer L. 1990. In vivo anterograde and retrograde axonal transport of the fluorescent rhodamine-dextran-amine, Fluoro-Ruby, within the CNS. Brain Res 526:127-134.
87. Shammah-Lagnado SJ, Alheid GF, Heimer L. 1996. Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol 376:489-507.
88. Shammah-Lagnado SJ, Santiago AC. 1999. Projections of the amygdalopiriform transition area (APir). A PHA-L study in the rat. Ann N Y Acad Sci 877:655-660.
89. Somerville LH, Whalen PJ, Kelley WM. 2010. Human bed nucleus of the stria terminalis indexes hypervigilant threat monitoring. Biol Psychiatry 68:416-424.
90. Squire LR. 1993. The hippocampus and spatial memory. Trends Neurosci 16:56-57.
91. Sullivan GM, Apergis J, Bush DEA, Johnson LR, Hou M, LeDoux JE. 2004. Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses eliected by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128:7-14.
92. Sun N, Roberts L, Cassell MD. 1991. Rat central amygdaloid nucleus projections to the bed nucleus of the stria terminalis. Brain Res Bull 27:651-662.
93. Szucs A, Berton F, Sanna PP, Francesconi W. 2012. Excitability of jcBNST neurons is reduced in alcohol-dependent animals during protracted alcohol withdrawal. PLoS One 7:e42313.
94. Turner BM, Mishikin M, Knapp M. 1980. Organization of the amygdaopetal projections from modality-specific cortical association areas in the monkey. J Comp Neurol 191:515-543.
95. Veinante P, Stoeckel ME, Lasbennes F, Freund-Mercier MJ. 2003. c-Fos and peptide immunoreactivities in the central extended amygdala of morphine-dependent rats after naloxone-precipitated withdrawal. Eur J Neurosci 18:1295-1305.
96. Vercelli A, Repici M, Garbossa D, Grimaldi A. 2000. Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51:11-28.
97. Walker DL, Davis M. 1997. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17:9375-9383.
98. Walker JR, Ahmed SH, Gracy KN, Koob GF. 2000. Microinjections of an opiate receptor antagonist into the bed nucleus of the stria terminalis suppress heroin self-administration in dependent rats. Brain Res 854:85-92.
99. Walter A, Mai JK, Lanta L, Gorcs T. 1991. Differential distribution of immunohistochemical markers in the bed nucleus of the stria terminalis in the human brain. J Chem Neuroanat 4:281-298.
100. Webster MJ, Bachevalier J, Ungerleider LG. 1993. Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. J Comp Neurol 335:73-91.
101. Weller KL, Smith DA. 1982. Afferent connections to the bed nucleus of the stria terminalis. Brain Res 232:255-270.
102. Zahm DS. 1998. Is the caudomedial shell of the nucleus accumbens part of the extended amygdala? A consideration of connections. Crit Rev Neurobiol 12:245-265.
103. Zahm DS, Jensen SL, Williams ES, Martin JR 3rd. 1999. Direct comparison of projections from the central amygdaloid region and nucleus accumbens shell. Eur J Neurosci 11:1119-1126.
104. Zimmerman JM, Maren S. 2011. The bed nucleus of the stria terminalis is required for the expression of contextual but not auditory freezing in rats with basolateral amygdala lesions. Neurobiol Learn Mem 95:199-205.