Evidence for coordinated functional activity within the extended amygdala of non-human and human primates

NeuroImage

Volumn 61, Issue 4, 2012, Pages 1059-1066

  Oler, Jonathan A ^a   Birn, Rasmus M ^a   Patriat, Rémi ^a   Fox, Andrew S ^b   Shelton, Steven E ^a   Burghy, Cory A ^b   Stodola, Diane E ^b   Essex, Marilyn J ^a   Davidson, Richard J ^a,b   Kalin, Ned H ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Bed nucleus of the stria terminalis; Central nucleus; Connectivity; Human; Resting state fMRI; Rhesus macaque

Indexed keywords

ADOLESCENT; ADULT; AMYGDALOID NUCLEUS; ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CENTRAL NUCLEUS (AMYGDALA); CHILD; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL NEUROIMAGING; HUMAN; IMAGE ANALYSIS; IMAGE DISPLAY; IN VIVO STUDY; MALE; NEUROANATOMY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRESCHOOL CHILD; PRIORITY JOURNAL; REST; RHESUS MONKEY; SCHOOL CHILD; STRIA TERMINALIS;

ADOLESCENT; AMYGDALA; ANIMALS; ANXIETY; CHILD; FEAR; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS;

EID: 84861330157     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.03.045     Document Type: Article

References (67)

1. Aggleton J.P. The amygdala. A Functional Analysis 2000.
2. Alheid G.F. Extended amygdala and basal forebrain. Ann. N.Y. Acad. Sci. 2003, 985:185-205.
3. Alheid G.F., Heimer L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 1988, 27:1-39.
4. Alvarez R.P., Chen G., Bodurka J., Kaplan R., Grillon C. Phasic and sustained fear in humans elicits distinct patterns of brain activity. Neuroimage 2010, 55:389-400.
5. Amaral D.G., Price J.L., Pitkänen A., Carmichael S.T. Anatomical organization of the primate amygdaloid complex. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction 1992, 1-66.
6. Bauman M.D., Amaral D.G. The distribution of serotonergic fibers in the macaque monkey amygdala: an immunohistochemical study using antisera to 5-hydroxytryptamine. Neuroscience 2005, 136:193-203.
7. Bupesh M., Abellan A., Medina L. Genetic and experimental evidence supports the continuum of the central extended amygdala and a mutiple embryonic origin of its principal neurons. J. Comp. Neurol. 2011, 519:3507-3531.
8. Cassell M.D. The amygdala: myth or monolith?. Trends Neurosci. 1998, 21:200-201.
9. Christian B.T., Fox A.S., Oler J.A., Vandehey N.T., Murali D., Rogers J., Oakes T.R., Shelton S.E., Davidson R.J., Kalin N.H. Serotonin transporter binding and genotype in the nonhuman primate brain using [C-11]DASB PET. Neuroimage 2009, 47:1230-1236.
10. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
11. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35:105-135.
12. de Olmos J.S., Heimer L. The concepts of the ventral striatopallidal system and extended amygdala. Advancing from the Ventral Striatum to the Extended Amygdala: Implications for Neuropsychiatry and Drug Abuse 1999, 1-32. The New York Academy of Sciences, New York. J.F. McGinty (Ed.).
13. De Olmos J.S., Ingram W.R. The projection field of the stria terminalis in the rat brain. An experimental study. J. Comp. Neurol. 1972, 146:303-334.
14. Di Martino A., Scheres A., Margulies D.S., Kelly A.M., Uddin L.Q., Shehzad Z., Biswal B., Walters J.R., Castellanos F.X., Milham M.P. Functional connectivity of human striatum: a resting state fMRI study. Cereb. Cortex 2008, 18:2735-2747.
15. Dong H.W., Petrovich G.D., Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 2001, 38:192-246.
16. Duvarci S., Bauer E.P., Pare D. The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J. Neurosci. 2009, 29:10357-10361.
17. Essex M.J., Shirtcliff E.A., Burk L.R., Ruttle P.L., Klein M.H., Slattery M.J., Kalin N.H., Armstrong J.M. Influence of early life stress on later hypothalamic-pituitary-adrenal axis functioning and its covariation with mental health symptoms: a study of the allostatic process from childhood into adolescence. Dev. Psychopathol. 2011, 23:1039-1058.
18. Fox A.S., Shelton S.E., Oakes T.R., Davidson R.J., Kalin N.H. Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS One 2008, 3:e2570.
19. Freedman L.J., Shi C. Monoaminergic innervation of the macaque extended amygdala. Neuroscience 2001, 104:1067-1084.
20. Freese J.L., Amaral D.G. Neuroanatomy of the primate amygdala. The Human Amygdala 2009, 3-42. Guilford, New York. P.J. Whalen, E.A. Phelps (Eds.).
21. Fudge J.L., Tucker T. Amygdala projections to central amygdaloid nucleus subdivisions and transition zones in the primate. Neuroscience 2009, 159:819-841.
22. Heimer L. A new anatomical framework for neuropsychiatric disorders and drug abuse. Am. J. Psychiatry 2003, 160:1726-1739.
23. Heimer L., Van Hoesen G.W. The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci. Biobehav. Rev. 2006, 30:126-147.
24. Heimer L., Harlan R.E., Alheid G.F., Garcia M.M., de Olmos J. Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders. Neuroscience 1997, 76:957-1006.
25. Heimer L., de Olmos J.S., Alheid G.F., Pearson J., Sakamoto N., Shinoda K., Marksteiner J., Switzer Iii R.C. Chapter II. The human basal forebrain. Part II. Handbook of Chemical Neuroanatomy 1999, 57-226. Elsevier. F.E. Bloom, T. Hökfelt (Eds.).
26. Innis R.B., Cunningham V.J., Delforge J., Fujita M., Gjedde A., Gunn R.N., Holden J., Houle S., Huang S.C., Ichise M., Iida H., Ito H., Kimura Y., Koeppe R.A., Knudsen G.M., Knuuti J., Lammertsma A.A., Laruelle M., Logan J., Maguire R.P., Mintun M.A., Morris E.D., Parsey R., Price J.C., Slifstein M., Sossi V., Suhara T., Votaw J.R., Wong D.F., Carson R.E. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J. Cereb. Blood Flow Metab. 2007, 27:1533-1539.
27. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
28. Jo H.J., Saad Z.S., Simmons W.K., Milbury L.A., Cox R.W. Mapping sources of correlation in resting state FMRI, with artifact detection and removal. Neuroimage 2010, 52:571-582.
29. Johnson J.B. Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 1923, 35:337-481.
30. Kalin N.H., Shelton S.E. Nonhuman primate models to study anxiety, emotion regulation, and psychopathology. Ann. N. Y. Acad. Sci. 2003, 1008:189-200.
31. Kalin N.H., Shelton S.E., Fox A.S., Oakes T.R., Davidson R.J. Brain regions associated with the expression and contextual regulation of anxiety in primates. Biol. Psychiatry 2005, 58:796-804.
32. Kelly C., Uddin L.Q., Shehzad Z., Margulies D.S., Castellanos F.X., Milham M.P., Petrides M. Broca's region: linking human brain functional connectivity data and non-human primate tracing anatomy studies. Eur. J. Neurosci. 2010, 32:383-398.
33. Klingler J., Gloor P. The connections of the amygdala and of the anterior temporal cortex in the human brain. J. Comp. Neurol. 1960, 115:333-369.
34. LeDoux J. The amygdala. Curr. Biol. 2007, 17:R868-R874.
35. Luyten L., Casteels C., Vansteenwegen D., van Kuyck K., Koole M., Van Laere K., Nuttin B. Micro-positron emission tomography imaging of rat brain metabolism during expression of contextual conditioning. J. Neurosci. 2012, 32:254-263.
36. Ma L., Worsley K.J., Evans A.C. Variability of spatial location of activation in fMRI and PET CBF images. Neuroimage 1999, 9:S178.
37. Machado C.J., Bachevalier J. Non-human primate models of childhood psychopathology: the promise and the limitations. J. Child Psychol. Psychiatry 2003, 44:64-87.
38. Mai J.K., Assheuer J., Paxinos G. Atlas of the Human Brain 2003, Elsevier Academic Press, San Diego. 2nd ed.
39. Margulies D.S., Kelly A.M., Uddin L.Q., Biswal B.B., Castellanos F.X., Milham M.P. Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 2007, 37:579-588.
40. Martin L.J., Powers R.E., Dellovade T.L., Price D.L. The bed nucleus-amygdala continuum in human and monkey. J. Comp. Neurol. 1991, 309:445-485.
41. McDonald A.J. Cell types and intrinsic connections of the amygdala. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction 1992, 67-96. Wiley-Liss, New York. J.P. Aggelton (Ed.).
42. McDonald A.J. Is there an amygdala and how far does it extend? An anatomical perspective. Ann. N.Y. Acad. Sci. 2003, 985:1-21.
43. Mobbs D., Yu R., Rowe J.B., Eich H., FeldmanHall O., Dalgleish T. Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20582-20586.
44. Nagy F.Z., Pare D. Timing of impulses from the central amygdala and bed nucleus of the stria terminalis to the brain stem. J. Neurophysiol. 2008, 100:3429-3436.
45. Oler J.A., Fox A.S., Shelton S.E., Rogers J., Dyer T.D., Davidson R.J., Shelledy W., Oakes T.R., Blangero J., Kalin N.H. Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature 2010, 466:864-868.
46. O'Rourke H., Fudge J.L. Distribution of serotonin transporter labeled fibers in amygdaloid subregions: implications for mood disorders. Biol. Psychiatry 2006, 60:479-490.
47. Park J., Wheeler R.A., Fontillas K., Keithley R.B., Carelli R.M., Wightman R.M. Catecholamines in the bed nucleus of the stria terminalis reciprocally respond to reward and aversion. Biol. Psychiatry 2012, 71:327-334.
48. Paxinos G., Mai J.K. The Human Nervous System 2004, Elsevier Science, Amsterdam. 2nd ed.
49. Paxinos G., Huang X., Petrides M., Toga A. The Rhesus Monkey Brain in Stereotaxic Coordinates 2009, Academic Press, San Diego. 2nd ed.
50. Pitkänen A. Connectivity of the rat amygdaloid complex. The Amygdala. A Functional Analysis 2000, 31-117. Oxford University Press, New York. J.P. Aggleton (Ed.).
51. Price J.L., Amaral D.G. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J. Neurosci. 1981, 1:1242-1259.
52. Price J.L., Russchen F.T., Amaral D.G. The limbic region II: the amygdaloid complex. Handbook of Chemical Neuroanatomy 1987, 279-388. Elsevier, Amsterdam. A. Björkland, T. Hökfelt, L.W. Swanson (Eds.).
53. Regev L., Neufeld-Cohen A., Tsoory M., Kuperman Y., Getselter D., Gil S., Chen A. Prolonged and site-specific over-expression of corticotropin-releasing factor reveals differential roles for extended amygdala nuclei in emotional regulation. Mol. Psychiatry 2011, 16:714-728.
54. Roy A.K., Shehzad Z., Margulies D.S., Kelly A.M., Uddin L.Q., Gotimer K., Biswal B.B., Castellanos F.X., Milham M.P. Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 2009, 45:614-626.
55. Shehzad Z., Kelly A.M., Reiss P.T., Gee D.G., Gotimer K., Uddin L.Q., Lee S.H., Margulies D.S., Roy A.K., Biswal B.B., Petkova E., Castellanos F.X., Milham M.P. The resting brain: unconstrained yet reliable. Cereb. Cortex 2009, 19:2209-2229.
56. The Amygdala in Brain Function: Basic and Clinical Applications 2003, The New York Academy of Sciences, New York. P. Shinnick-Gallagher, A. Pitkanen, A. Shekhar, L. Cahill (Eds.).
57. Sink K.S., Walker D.L., Freeman S.M., Flandreau E.I., Ressler K.J., Davis M. Effects of continuously enhanced corticotropin releasing factor expression within the bed nucleus of the stria terminalis on conditioned and unconditioned anxiety. Mol. Psychiatry 2012, 2012 (Electronic publication ahead of print, Jan 31). 10.1038/mp.2011.188.
58. Solano-Castiella E., Anwander A., Lohmann G., Weiss M., Docherty C., Geyer S., Reimer E., Friederici A.D., Turner R. Diffusion tensor imaging segments the human amygdala in vivo. Neuroimage 2010, 49:2958-2965.
59. Somerville L.H., Whalen P.J., Kelley W.M. Human bed nucleus of the stria terminalis indexes hypervigilant threat monitoring. Biol. Psychiatry 2010, 68:416-424.
60. Somerville L.H., Wagner D.D., Wig G.S., Moran J.M., Whalen P.J., Kelley W.M. Interactions between transient and sustained neural signals support the generation and regulation of anxious emotion. Cereb. Cortex 2012, 2012 (Electronic publication ahead of print, Jan 16).
61. Straube T., Mentzel H.J., Miltner W.H. Waiting for spiders: brain activation during anticipatory anxiety in spider phobics. Neuroimage 2007, 37:1427-1436.
62. Swanson L.W., Petrovitch G.D. What is the amygdala?. Trends Neurosci. 1998, 21:323-330.
63. Tai C., Chatziioannou A., Siegel S., Young J., Newport D., Goble R.N., Nutt R.E., Cherry S.R. Performance evaluation of the microPET P4: a PET system dedicated to animal imaging. Phys. Med. Biol. 2001, 46:1845-1862.
64. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447:83-86.
65. Walker D.L., Davis M. Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer. Brain Struct. Funct. 2008, 213:29-42.
66. The Human Amygdala 2009, Guilford, New York. P.J. Whalen, E.A. Phelps (Eds.).
67. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20:45-57.