42 Motivation
require that an animal respond to a threat with specific be-
haviors. Turtles withdraw into their hard shells; porcupines
raise their sharp quills; and grasshoppers retreat a short dis-
tance and then become immobile when they are threatened.
These behaviors can be inflexible, but they are often sensitive
to feedback. Unlike primary defensive strategies, which are
permanently employed, these defensive behaviors are trig-
gered by a fear-driven motivational system.
The Pervasiveness of Fear in Motivated Behavior
Fear modulates other motivational systems. Animals that
miss a meal or a mating opportunity usually live to eat or
mate another day. Animals that fail to defend usually have no
further reproductive chances. Therefore, fear takes prece-
dence over other motivational systems. One of the first quan-
titative measures of fear was the ability to suppress food
intake (Estes & Skinner, 1941). The effects of fear on feed-
ing can also be subtle. As described earlier, Fanselow et al.
(1988) demonstrated that rats adjust the size and frequency
of meals in relation to shock density. Animals were housed
in an environment that had a safe burrow. The burrow was
attached to an area with a grid floor, and brief shock was
delivered to this area on a random schedule. The rat could
obtain food only if it risked venturing onto the grid floor area
to eat. The results suggest that with increasing shock density,
rats take fewer, but larger, meals. Thus, fear motivation
seems to modulate foraging behaviors (i.e., feeding motiva-
tion). Similarly, rats cease foraging, retreat to a burrow, and
delay further foraging for hours after they encounter a cat
near the entrance of the burrow (Blanchard & Blanchard,
1989), and monkeys seem reluctant to reach over a snake to
obtain food (Mineka & Cook, 1988). Fear also influences
sexual motivation. For example, female stickleback fish pro-
duce few offspring with a male conspecific that displays in-
appropriate territorial aggression toward them (Hollis, Pharr,
Dumas, Britton, & Field, 1997). During the aggressive act the
female may be both injured and frightened by the male, and
females often retreat from the vicinity when attacked. Thus,
fear modulates sexual motivation by disrupting or delaying
reproductive opportunities.
Factors Governing Initiation of Fear
An effective behavioral defensive strategy requires that ani-
mals identify threats with sufficient time to perform the ap-
propriate defensive responses. Numerous types of stimuli can
signal danger and activate fear motivational systems. These
stimuli can be divided into three functional classes: learned
fear stimuli, innate fear stimuli, and observational learning
and fear stimuli.Learned Fear StimuliFear is rapidly learned and measured in the laboratory
(Fanselow, 1994); it has direct clinical relevance (Bouton,
Mineka, & Barlow, 2001); and it has become a standard
method for exploring the behavioral processes and neural
mechanisms of learning. In the prototypical laboratory ex-
periment, a rat is placed in a chamber where it is presented
with a tone that is followed by a brief aversive foot shock.
Later during a test session, the rat is reexposed to either the
conditioning chamber or the tone. During this reexposure
the rat will engage in behaviors that are characteristic of
fear. With this preparation the tone and the chamber, or
context, serve as conditional stimuli (CSs). They were orig-
inally neutral stimuli, but after they were paired with an
unconditional stimulus (US), the foot shock, the animal re-
sponded to the CS in a fearful manner. Such responses to the
CSs are called conditional responses (CRs). These fear CRs
occur specifically to the shock-paired stimuli, and these
responses are used as measures of learning in Pavlovian
experiments (see also chapter by Miller and Grace in this
volume). To date, Pavlovian fear has been characterized
with several CRs such as defensive freezing, reflex facilita-
tion, heart rate, blood pressure, conditional suppression,
conditional analgesia, and vocalizations (see Fendt &
Fanselow, 1999, for review).
Animals can learn to associate a threat with numerous
classes of CSs. Auditory cues, visual cues, olfactory cues,
and tactile cues can all become fear CSs with the appro-
priate training regime. However, the nature of the CS is not
arbitrary because animals are known to exhibitselective as-
sociations. This phenomenon is best exemplified by an ex-
periment performed by Garcia and Koelling (1966) in which
rats were presented with a compound CS. The compound CS
consisted of auditory, visual, and flavor cues: a buzzing noise,
a blinking light, and the taste of saccharin, respectively. Dur-
ing training trials the presentation of the compound CS was
followed by the occurrence of footshock. During test ses-
sions, rats exhibited fear reaction to the auditory and visual
cue, and not to the flavor cue. Thus, this experiment suggests
that in the rat visual and auditory cues are more readily asso-
ciated with threat. Asymmetry in this sort of stimulus selec-
tion appears ubiquitous. Similar selective associations have
been demonstrated in the pigeon (Foree & Lolordo, 1973).
Further, tone onset is more readily associated with danger
than light onset, which is more readily associated with safety