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The Journal of Neuroscience, March 21, 2007, 27(12):3295-3304; doi:10.1523/JNEUROSCI.4765-06.2007
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Development/Plasticity/Repair
Amygdala Gene Expression Correlates of Social Behavior in Monkeys Experiencing Maternal Separation
Michael J. Sabatini,1,3 Philip Ebert,7,8 David A. Lewis,1,2 Pat Levitt,1,7,8 Judy L. Cameron,1,4,5 andKároly Mirnics1,6,8 Departments of 1Psychiatry, 2Neuroscience, and 3Neurobiology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, 4Departments of Physiology and Pharmacology and Behavioral Neuroscience, Oregon Health & Science University, Portland, Oregon 97239-3098, 5Oregon National Primate Research Center, Beaverton, Oregon 97006-3448, and Departments of 6Psychiatry and 7Pharmacology and 8Vanderbilt Kennedy Center for Human Development, Vanderbilt University, Nashville, Tennessee 37203
Correspondence should be addressed to Karoly Mirnics, Department of Psychiatry, Vanderbilt University, 8130A MRB III, 465 21st Avenue South, Nashville, TN 37203. Email: karoly.mirnics{at}vanderbilt.edu
Children exposed to early parental loss from death or separation carry a greater risk for developing future psychiatric illnesses, such as major depression and anxiety. Monkeys experiencing maternal separation at 1 week of age show fewer social behaviors and an increase in self-comforting behaviors (e.g., thumb sucking) over development, whereas in contrast, monkeys experiencing maternal separation at 1 month of age show increased seeking of social comfort later in life. We sought to identify neural systems that may underlie these stress-induced behavioral changes by examining changes in mRNA content in amygdala tissue collected from 1 week separated, 1 month separated, and maternally reared infants at 3 months of age. mRNA from the right medial temporal lobe, primarily the amygdala, was analyzed using Affymetrix U133A 2.0 arrays. One gene, guanylate cyclase 1
3 (GUCY1A3), showed differential expression between the 1 week and maternally reared groups and the 1 week and 1 month groups; these changes were confirmed by in situ hybridization. The expression of this gene was positively correlated with acute social-comforting behavior (r = 0.923; p = 0.001) and longer-term close social behavior (r = 0.708; p = 0.015) and negatively correlated with self-comforting behaviors (r = –0.88; p < 0.001). Additional in situ hybridization studies of GUCY1A3 in normal monkeys showed that this gene is expressed at adult levels by 1 week of age and that its expression is greater in the amygdala than all other brain areas examined. We conclude that GUCY1A3 may contribute to the altered behavioral phenotypes that are differentially displayed depending on the age at which macaque infants experience an early-life stress.
Key words: DNA microarray; gene expression; amygdala; maternal separation; in situ hybridization; behavior; rhesus macaque; guanylate cyclase
Received Nov. 1, 2006; revised Jan. 3, 2007; accepted Feb. 12, 2007.
Correspondence should be addressed to Karoly Mirnics, Department of Psychiatry, Vanderbilt University, 8130A MRB III, 465 21st Avenue South, Nashville, TN 37203. Email: karoly.mirnics{at}vanderbilt.edu
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J. Neurosci. 2007 27: i.[Full Text]
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