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Behavioral
Neuroscience
2001,
Vol.
115,
No. 3,
710-717
Copyright
2001
by the
American
Psychological Association, Inc.
0735-7044/01/S5.00
DOI:
10.1037//0735-7044.115.3.710
Conditioned Brain-Stimulation Reward Attenuates
the
Acoustic
Startle Reflex
in
Rats
Stephan
Steidl
University
of
Toronto
Liang
Li
Peking
University
John
S.
Yeomans
University
of
Toronto
The
acoustic startle reflex (ASR)
in
rats
is
attenuated
by a
light paired with food
or, in
humans,
by
"pleasant"
pictures. Rats were trained
to
barpress
for
lateral hypothalamus (LH) stimulation.
ASR
amplitudes
were then measured
at 4
intensities,
with
or
without
a
light. Control rats that
did not
receive
brain-stimulation
reward (BSR) showed
initially
lower
ASR
amplitudes
than
did
rats exposed
to
BSR,
but
both groups responded
similarly
with
or
without light. Next, experimental rats were given
BSR in the
presence
of
light
but not in its
absence.
After
conditioning,
ASR
amplitudes were reduced,
and ASR
thresholds
were raised
by a
mean
of 2.6 dB in the
light
but
remained
at
preconditioning levels
without
light.
No
such change
was
found
for
control
rats
or
rats with placements outside
the LH.
The
acoustic startle reflex (ASR) involves
a
rapid contraction
of
skeletal
muscles throughout
the
body after
an
unexpected
and
intense
acoustic stimulus.
The
magnitude
of the ASR is
modulated
by
changes
in the
perceptual
and
emotional state
of the
animal.
In
the
fear-potentiated startle paradigm,
the ASR is
enhanced
in the
presence
of a cue
predicting
an
aversive footshock (Brown, Kalish,
&
Farber, 1951; Davis,
1989).
The
amplitude
of the
eyeblink
component
of ASR in
humans
is
enhanced
in the
presence
of
emotionally
aversive pictures compared with emotionally neutral
pictures
(Lang, Bradley,
&
Cuthbert,
1990). Humans with post-
traumatic stress disorder show elevated startle responses (Butler
et
al.,
1990).
Startle provides
a
sensitive measure
of
emotional states,
variously
called "fear,"
"panic,"
"stress,"
or
"anxiety,"
that
is
useful
in
evaluating
the
effects
of
drugs
and in
studying neural
circuits
for
these states (Davis, Falls, Campeau,
&
Kim, 1993;
Frankland,
Josselyn, Bradwejn,
Vaccarino,
&
Yeomans, 1997;
Walker
&
Davis, 1997).
The
amplitude
of the
eyeblink component
of ASR in
humans
is
attenuated
in the
presence
of
pictures
described
as
emotionally
positive
(Lang
et
al.,
1990).
Of
most relevance
to the
present study,
ASR in
rats
was
reduced
in the
presence
of a
light that
had
previously
been paired with food (Schmid, Koch,
&
Schnitzler,
Stephan
Steidl
and
John
S.
Yeomans, Department
of
Psychology, Uni-
versity
of
Toronto, Toronto, Ontario, Canada; Liang
Li,
Department
of
Psychology,
Peking
University,
Peking,
People's
Republic
of
China.
This
research
was
supported
by
National Sciences
and
Engineering
Research Council
of
Canada Grant
A
7077
and
Medical Research Council
of
Canada Grant MT14624.
We
thank David Bush
and
James Fulton
for
technical
assistance.
Correspondence concerning this article should
be
addressed
to
John
S.
Yeomans, Department
of
Psychology, University
of
Toronto,
100 St.
George Street, Toronto, Ontario
M5S
3G3, Canada. Electronic mail
may be
sent
to
yeomans@psych.utoronto.ca.
1995). These
effects
have been called "pleasure-attenuated star-
tle."
In the
latter study, baseline
ASR
amplitudes were obtained
without
a
light
cue
from food-
and
water-deprived rats. Rats
in the
conditioned
group were trained
to
associate
a
neutral stimulus
(conditioned
stimulus [CS], light) with food (unconditioned stim-
ulus).
Conditioning took place
in a
dark chamber
in
which food
was
presented during
a
4-min
period with
the
light turned
on.
Control rats spent
the
same amount
of
time
in
their home
cages,
receiving
the
same amount
of
food
at
irregular points
in
time.
No
trials without
a
light
cue
(CS—)
were presented after conditioning,
and
conditioning took place
in a
different
context than subsequent
testing.
ASR was
significantly attenuated
in the
presence
of
con-
stant
light
in the
conditioned rats compared with preconditioning
baselines, whereas controls showed
no
significant difference ver-
sus
baseline.
The
main goal
of the
present study
was to
extend
the
phenom-
enon
of
reward-attenuated startle from conditioned food reward
to
conditioned brain-stimulation reward (BSR). Rats prefer
BSR
over
food
in
some conditions, suggesting that
BSR can be
more reward-
ing
(Routtenberg
&
Lindy, 1965).
No
deprivation
is
required
in
BSR
experiments. Controls were added
to (a)
evaluate
the
uncon-
ditioned effects
of
light,
(b)
control
the
environment within
and
between groups,
and (c)
estimate
ASR
sensitivity changes result-
ing
from
the
conditioned reward
by the
shift
in
decibel
threshold.
Method
Subjects
Thirteen
male Wistar rats
(Rattus
norvegicus) weighing
a
mean
of 350 g,
obtained
from
Charles River Canada (St. Constant, Quebec), were individ-
ually
housed
on a
12-hr
light-dark
cycle.
Food
and
water were available
in
the
home cages throughout
the
experiment.
The
University
of
Toronto
Animal
Care Committee, following
the
guidelines
of the
Canadian Council
of
Animal
Care,
approved
the
care
of
rats used
in
this study.
710
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