SELECTIVE BREEDING FOR DEFICIENT SENSORIMOTOR GATING IS
ACCOMPANIED BY INCREASED PERSEVERATION IN RATS
F. FREUDENBERG,
1
M. DIECKMANN,
1
S. WINTER,
1
M. KOCH AND K. SCHWABE
1
*
Brain Research Institute, Department of Neuropharmacology, Univer-
sity of Bremen, P.O. Box 33 04 40, 28334 Bremen, Germany
Abstract—Prepulse inhibition (PPI) of the acoustic startle
response is a measure of sensorimotor gating that is defi-
cient in some neuropsychiatric disorders, such as schizo-
phrenia and Tourette’s syndrome. Experimentally induced
PPI deficits in rats are regarded as endophenotype to study
the biological mechanisms and therapeutic strategies of
these disorders. We have recently shown that selectively
breeding rats for high and low PPI levels, respectively, leads
to groups with different PPI performance that remains stable
from the second generation on. We here tested whether the
low PPI is accompanied by other behavioral deficits.
Different spatial and operant learning paradigms were
used to assess rats’ learning and memory abilities as well as
their behavioral flexibility. In the delayed alternation T-maze
task the two groups did not differ in task acquisition and
working memory. Rats with low PPI showed enhanced per-
severation during switching between an egocentric and allo-
centric radial maze task. Enhanced perseveration was also
found in an operant behavioral task, where different de-
mands, i.e. a different number of lever presses for a pellet-
reward, were assigned to and switched between two levers of
a Skinner box. Rats with low PPI stayed longer at the ineffec-
tive lever before switching, thus being less able to adjust
their behavior to changing reward values. Additionally, PPI
low rats had a higher breakpoint value during a progressive
ratio-schedule of reinforcement.
Rats selectively bred for low PPI showed some cognitive
deficits that are apparent in a number of psychiatric disor-
ders with deficient information processing. Specifically in
both, spatial and operant behavioral paradigms, PPI low rats
are deteriorated in their ability to modulate behavior based
upon new changing information. They may thus provide a
non-pharmacological model that can be used to evaluate new
therapeutic strategies ranging from pharmacological treat-
ment to functional neurosurgery. © 2007 IBRO. Published by
Elsevier Ltd. All rights reserved.
Key words: prepulse inhibition, schizophrenia, Tourette’s
syndrome, animal model, endophenotype, learning and
memory.
The concept of the endophenotype or intermediate pheno-
type (Gould and Gottesman, 2006; Meyer-Lindenberg and
Weinberger, 2006) proposes a biological basis for complex
neuropsychiatric diseases that can be studied by using
phenotypes that are related to both the clinical symptoms
but also to more basic biological mechanisms. Deficits in
early information processing or sensorimotor gating are
considered core features of schizophrenia and have been
linked to psychotic symptom formation and disturbed cog-
nitive function in these patients (Cadenhead et al., 2002;
Light and Braff, 2005). Deficient sensorimotor gating can
be operationalized by reduced prepulse inhibition (PPI) of
the startle reaction, which can be measured in humans and
animals by using virtually the same approaches. Deficit in
PPI is therefore used as an endophenotype marker to
study the etiology and pathophysiology underlying the psy-
chotic state at the level of animal neurobiology (Braff et al.,
2001b). In addition to these sensorimotor gating deficits,
disturbed working memory and executive function are con-
sidered core features of schizophrenia and thus serve as
endophenotypes for this disorder (Hutton et al., 1998; We-
ickert et al., 2000; Badcock et al., 2005). Interestingly, in
healthy humans, PPI performance has been found to be
associated with cognitive functions (Bitsios and Giakou-
maki, 2005).
We have recently shown that selective breeding in
Wistar rats for high and low PPI levels leads to a segre-
gation of two rat lines with significantly different PPI al-
ready in the first two generations. The PPI deficit in these
rats was ameliorated with antipsychotic compounds mak-
ing these rats an interesting model with possible predictive
validity for the screening of antipsychotic drugs (Hadam-
itzky et al., 2007). We here addressed the question,
whether these rats show other comorbid features or cog-
nitive deficits related to psychiatric disorders with disturbed
information processing. For this purpose rats were tested
in different spatial and operant paradigms to assess their
learning and memory abilities as well as their behavioral
flexibility. First, rats were tested in the four-arm baited
eight-arm radial maze task, which provides measures of
both reference and working memory (Olton, 1979; Olton
and Papas, 1979). Thereafter, they were trained in an
egocentric strategy, where they had to navigate relative to
1
Present address: Department of Neurosurgery, Medical University,
MHH, Carl-Neuberg-Str. 1, D-30625 Hannover, Germany (S. Winter,
K. Schwabe); Department of Molecular Neurobiology, Max-Planck
Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg,
Germany (F. Freudenberg); Department of Molecular Neurodegenera-
tion, Institute for Physiological Chemistry and Pathobiochemistry, Jo-
hannes Gutenberg-University, 55099 Mainz, Germany (M. Dieck-
mann).
*Correspondence to: K. Schwabe, Department of Neurosurgery,
Medical University, MHH, Carl-Neuberg-Str. 1, D-30625 Hannover,
Germany.
E-mail address: schwabe.kerstin@mh-hannover.de (K. Schwabe).
Abbreviations: ANOVA, analysis of variance; ASR, acoustic startle
response; FR, fixed ratio; ITI, intertrial interval; PE, perseveration
error; PLE, perseveration-like error; PPI, prepulse inhibition; RE, re-
maining error; RME, reference memory error; SPL, sound pressure
level; WCST, Wisconsin Card Sorting Test; WME, working memory
error.
Neuroscience 148 (2007) 612– 622
0306-4522/07$30.00+0.00 © 2007 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2007.06.034
612