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PMID: 16093315 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Beyond affect: a role for genetic variation of the serotonin transporter in neural activation during a cognitive attention task.

Canli T, Omura K, Haas BW, Fallgatter A, Constable RT, Lesch KP

Abstract

Prior work has highlighted the role of genetic variation within the repetitive sequence in the transcriptional control region of the serotonin (5-HT) transporter gene (5-HTT, SLC6A4) in modulating amygdala and prefrontal activation to negative emotional stimuli. However, these studies have not explicitly tested the assumption that the control condition (neutral baseline) does not itself produce changes in activation as a function of 5-HTT genotype. Using a fixation baseline condition, we show that variation in 5-HTT genotype is associated with differential activation to negative, positive, and neutral stimuli in limbic, striatal, and cortical regions. We replicate earlier reports of increased amygdala activation to negative, relative to neutral, stimuli, but then show that these differences are driven by decreased activation to neutral stimuli, rather than increased activation to negative stimuli, in carriers of the 5-HTT short allele. Using high-resolution structural images and automated processes to test for brain volume and gray matter density, we further report significant differences, as a function of 5-HTT genotype, in frontal cortical regions, anterior cingulate, and cerebellum. These functional and structural differences suggest a much broader role for 5-HT transport efficiency in brain processes than previously thought. 5-HTT genotype affects neural systems controlling affective, cognitive, and motor processes.

MeSH Terms
Analysis of Variance Attention/physiology Body Weights and Measures Brain/physiology,ultrastructure Female Genetic Variation Genotype Humans Magnetic Resonance Imaging Male Photic Stimulation Positron-Emission Tomography Protein Transport/physiology Psychomotor Performance Serotonin Plasma Membrane Transport Proteins/genetics,metabolism
Chemicals
SLC6A4 protein, human Serotonin Plasma Membrane Transport Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Canli Turhan
Department of Psychology and Graduate Program in Genetics, Stony Brook University, Stony Brook, NY 11794-2500, USA. turhan.canli@sunysb.edu
Omura Kazufumi
Haas Brian W
Fallgatter Andreas
Constable R Todd
Lesch Klaus Peter
References (45)
45 references, click to expand
  1. A functional genetic variation of the serotonin (5-HT) transporter affects 5-HT1A receptor binding in humans.
    J Neurosci. 2005 Mar 9;25(10):2586-90 PMID: 15758168
  2. The counting Stroop: an interference task specialized for functional neuroimaging--validation study with functional MRI.
    Hum Brain Mapp. 1998;6(4):270-82 PMID: 9704265
  3. Serotonin transporter genetic variation and the response of the human amygdala.
    Science. 2002 Jul 19;297(5580):400-3 PMID: 12130784
  4. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene.
    Science. 2003 Jul 18;301(5631):386-9 PMID: 12869766
  5. The amygdala: vigilance and emotion.
    Mol Psychiatry. 2001 Jan;6(1):13-34 PMID: 11244481
  6. Depression: perspectives from affective neuroscience.
    Annu Rev Psychol. 2002;53:545-74 PMID: 11752496
  7. Reduced volume of orbitofrontal cortex in major depression.
    Biol Psychiatry. 2002 Feb 15;51(4):273-9 PMID: 11958777
  8. The anatomy of melancholia--focal abnormalities of cerebral blood flow in major depression.
    Psychol Med. 1992 Aug;22(3):607-15 PMID: 1410086
  9. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression.
    Biol Psychiatry. 1999 May 1;45(9):1085-98 PMID: 10331101
  10. A susceptibility gene for affective disorders and the response of the human amygdala.
    Arch Gen Psychiatry. 2005 Feb;62(2):146-52 PMID: 15699291
  11. Subcortical and cortical brain activity during the feeling of self-generated emotions.
    Nat Neurosci. 2000 Oct;3(10):1049-56 PMID: 11017179
  12. The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division.
    Biol Psychiatry. 1998 Dec 15;44(12):1219-28 PMID: 9861465
  13. Contributions of anterior cingulate cortex to behaviour.
    Brain. 1995 Feb;118 ( Pt 1):279-306 PMID: 7895011
  14. A voxel-based morphometric study of ageing in 465 normal adult human brains.
    Neuroimage. 2001 Jul;14(1 Pt 1):21-36 PMID: 11525331
  15. Serotonin transporter polymorphism related to amygdala excitability and symptom severity in patients with social phobia.
    Neurosci Lett. 2004 May 27;362(3):189-92 PMID: 15158011
  16. Cognitive and emotional influences in anterior cingulate cortex.
    Trends Cogn Sci. 2000 Jun;4(6):215-222 PMID: 10827444
  17. Effect of sertraline on regional metabolic rate in patients with affective disorder.
    Biol Psychiatry. 1997 Jan 1;41(1):15-22 PMID: 8988791
  18. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI.
    Neuroimage. 2002 Jun;16(2):331-48 PMID: 12030820
  19. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold.
    Magn Reson Med. 1995 May;33(5):636-47 PMID: 7596267
  20. Linguistic threat activates the human amygdala.
    Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10456-9 PMID: 10468630
  21. Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits.
    Am J Med Genet B Neuropsychiatr Genet. 2004 May 15;127B(1):85-9 PMID: 15108187
  22. A double dissociation between mood states and personality traits in the anterior cingulate.
    Behav Neurosci. 2004 Oct;118(5):897-904 PMID: 15506872
  23. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression.
    Nat Neurosci. 2005 Jun;8(6):828-34 PMID: 15880108
  24. The future of genetic studies of complex human diseases.
    Science. 1996 Sep 13;273(5281):1516-7 PMID: 8801636
  25. An fMRI study of personality influences on brain reactivity to emotional stimuli.
    Behav Neurosci. 2001 Feb;115(1):33-42 PMID: 11256451
  26. Assessing the significance of focal activations using their spatial extent.
    Hum Brain Mapp. 1994;1(3):210-20 PMID: 24578041
  27. Neural and behavioral substrates of mood and mood regulation.
    Biol Psychiatry. 2002 Sep 15;52(6):478-502 PMID: 12361665
  28. Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter.
    Nat Neurosci. 2005 Jan;8(1):20-1 PMID: 15592465
  29. The cerebellar cognitive affective syndrome.
    Brain. 1998 Apr;121 ( Pt 4):561-79 PMID: 9577385
  30. Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression.
    Prog Brain Res. 2000;126:413-31 PMID: 11105660
  31. Neuroanatomical correlates of externally and internally generated human emotion.
    Am J Psychiatry. 1997 Jul;154(7):918-25 PMID: 9210741
  32. Brain activity during transient sadness and happiness in healthy women.
    Am J Psychiatry. 1995 Mar;152(3):341-51 PMID: 7864258
  33. A default mode of brain function.
    Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):676-82 PMID: 11209064
  34. Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex.
    J Cogn Neurosci. 1997 Fall;9(5):648-63 PMID: 23965122
  35. Limbic-cortical dysregulation: a proposed model of depression.
    J Neuropsychiatry Clin Neurosci. 1997 Summer;9(3):471-81 PMID: 9276848
  36. The anterior cingulate cortex. The evolution of an interface between emotion and cognition.
    Ann N Y Acad Sci. 2001 May;935:107-17 PMID: 11411161
  37. Attention, self-regulation and consciousness.
    Philos Trans R Soc Lond B Biol Sci. 1998 Nov 29;353(1377):1915-27 PMID: 9854264
  38. Neural circuits underlying emotional distress in humans.
    Ann N Y Acad Sci. 2004 Dec;1032:254-7 PMID: 15677422
  39. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region.
    Science. 1996 Nov 29;274(5292):1527-31 PMID: 8929413
  40. Evidence of a role for the 5-HTTLPR genotype in the modulation of motor response to antidepressant treatment.
    Psychopharmacology (Berl). 2005 Mar;178(2-3):303-8 PMID: 15322730
  41. The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm.
    Proc Natl Acad Sci U S A. 1990 Jan;87(1):256-9 PMID: 2296583
  42. Voxel-based morphometry--the methods.
    Neuroimage. 2000 Jun;11(6 Pt 1):805-21 PMID: 10860804
  43. Why voxel-based morphometry should be used.
    Neuroimage. 2001 Dec;14(6):1238-43 PMID: 11707080
  44. Lateralization of amygdala activation: a systematic review of functional neuroimaging studies.
    Brain Res Brain Res Rev. 2004 May;45(2):96-103 PMID: 15145620
  45. Gene-environment interaction and the genetics of depression.
    J Psychiatry Neurosci. 2004 May;29(3):174-84 PMID: 15173894
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-08-23
Epub
2005-00-10
Pages
12224-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1189322
Subset
IM
Grants
NCRR NIH HHS · M01 RR010710 · United States
NCRR NIH HHS · 5M01 RR 10710 · United States
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