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Behavior Genetics, Vol. 34, No. 3, May 2004 (© 2004)
QTL Analysis of Multiple Behavioral
Measures of Anxiety in Mice
Norman D. Henderson,
1,4
Maria Grazia Turri,
2
John C. DeFries,
3
and Jonathan Flint
2
Received 2 Dec. 2002—Final 31 July 2003
In a test battery consisting of an open-field arena, a light-dark box, a mirror-chamber box, an
elevated plus maze, and an elevated square maze, 1,671 mice were tested, generating over 100
putative measures of anxiety in rodents. Quantitative trait loci (QTL) analysis was carried out
on all measures, plus composite measures and phenotypic factor scores. Significant LOD scores
were found for QTL on 17 chromosomes, with large and consistent QTL behavioral effects on
chromosomes 1, 4, 7, 8, 14, 15, l8, and X. QTL on chromosomes 4 and 8 largely influence
locomotor activity in both home cages and novel environments, whereas QTL on chromosomes
1, 15, and 18 influence anxiety-related behaviors. Five genetically separable, cross-test dimen-
sions of anxiety could be identified: (i) the suppression of locomotor activity in low to moder-
ately anxiogenic regions of the tests; (ii) a shift toward proportionally less time and activity
spent in high-anxiogenic test areas; (iii) the suppression of rearing behavior; (iv) increased
latency to enter novel areas; (v) increased autonomic responses, as assessed by defecation and
urination. Patterns of QTL influence on cross-test composite scores were distinctive. For example,
the QTL on chromosome 1 strongly influenced safe-area locomotor activity (LOD = 35) and
autonomic responses (LOD = 16), whereas the QTL on chromosome 15 influenced the propor-
tion of activity in high-anxiogenic areas (LOD = 16), latency to enter novel areas (LOD = 36)
and rearing behavior (LOD = 57). Phenotypic factor analysis identified factors heavily loaded
on single tests, rather than cross-test factors. The use of factor analysis or within-test principal
components for data reduction before genetic analysis was less satisfactory than using genetic
dissection methods on the original measures and logically derived composites.
KEY WORDS: Open-field; light-dark box; elevated plus maze; elevated square maze; mirror chamber;
anxiety; activity; emotionality; autonomic responses; anxiogenic environments; rearing; risk taking; home
cage; quantitative trait loci (QTL); genetic dissection; chromosome; LOD scores; F2 mice; factor analysis.
INTRODUCTION
During the past decade we have been using molecular
mapping strategies to investigate the genetic architec-
ture responsible for individual behavioral differences
in the DeFries strains of mice (Flint et al., 1995; Turri
et al., 2001a, b). The DeFries strains are derived from
a cross of two inbred strains (BALB/cJ and C57/BL6)
that were selected for differences in open-field activity,
a test that is believed to model susceptibility to anxiety
in rodents. Thirty generations of artificial selection in
the open-field arena resulted in large activity differ-
ences among the lines, which persisted after 18 gener-
ations of random mating and 35+ generations of
inbreeding, that produced the six DeFries strains: two
high (H1 and H2), two low (L1 and L2), and two con-
trol lines (C1 and C2), that were not subject to selec-
tion (DeFries and Hegman, 1970; DeFries et al., 1978).
We have previously reported genetic mapping
experiments using F2 intercrosses between both the H1
and L1 strains and the H2 and L2 strains, using several
phenotypes to determine whether a common set of
genetic loci influence behavior in tests that are believed
1
Oberlin College, Oberlin, Ohio.
2
Wellcome Trust Centre for Human Genetics, Oxford, United
Kingdom.
3
Institute for Behavioral Genetics, University of Colorado, Boulder,
Colorado.
4
To whom correspondence should be addressed at Department of
Psychology, Oberlin College, Oberlin, Ohio 44074. Tel: 440-775-
7695; Fax: 440-775-8356. e-mail: nhenders@oberlin.edu