LEARNING AND MOTIVATION

ARTICLE NO.

27, 130150 (1996)

0008

A Behavior Systems Approach to Bidirectional

Excitatory Serial Conditioning
FRANCISCO J. SILVA, WILLIAM TIMBERLAKE,

AND

TERI L. KOEHLER

Indiana University
The present study explored bidirectional excitatory conditioning using the behavior
systems assumption that conditioned responding is related to a sequence of search
modes preceding and following the unconditioned stimulus. In Experiment 1a, rats
were initially trained with either a forward serial conditioned stimulus (CS) (FCSF
FCSI FCSN Food; the subscripts F, I, and N denote, respectively, elements temporally Far, Intermediate, and Near to food) or a backward serial CS (FoodBCSN
BCSI BCSF). In Experiment 1b, all rats received one of the 8-s elements of the serial
CS compounded with presentation of a novel lever and followed by food. Both forward
and backward procedures produced evidence that the elements of the serial CS differentially controlled types of search mode. The forward but not the backward procedure
also provided evidence for the conditioning of specific responses, which competed
for expression with lever-directed responding in the compound condition. The results
suggested several advantages of analyzing Pavlovian conditioning within a behavior
systems framework. q 1996 Academic Press, Inc.

Most traditional associative theories contend that forward pairings of a

conditioned and unconditioned stimulus (CSUS) produce excitatory associations, while backward pairings (USCS) typically do not (see Miller & Spear,
1985). However, a number of experiments using backward pairings have
supported the possibility of backward excitatory conditioning (Pavlov, 1932;
Wagner & Terry, 1975). For example, Tait and Saladin (1986) showed that
USCS pairings produced concurrent excitatory and inhibitory associations in
rabbit eyelid conditioning. Other experiments have suggested that the apparent
absence of backward excitatory conditioning may reflect the experimenters
choice of response and measure rather than a failure to form excitatory associ-

This research was supported by NSF Grants IBN-9121647 and 9408366. We thank Kathleen
Silva for comments on previous drafts of the manuscript and Jessica Rogers for assistance in
data collection. Reprint requests and correspondence should be addressed to William Timberlake,
Department of Psychology, Indiana University, Bloomington, Indiana 47405. E-mail: timberla@
indiana.edu.

130
0023-9690/96 $18.00
Copyright q 1996 by Academic Press, Inc.
All rights of reproduction in any form reserved.

AID

L&M 0928

/ ae01$$$$21

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

131

ations (see Hearst, 1989; Hemmes, Brown, & Cabeza de Vaca, 1994; Holland,
1984; Miller & Barnet, 1993; Matzel, Held, & Miller, 1988; Miller & Matzel,
1989; Spetch, Wilkie, & Pinel, 1981; Wagner & Brandon, 1989).
Despite the relatively sparse empirical evidence, excitatory backward conditioning is intuitively a reasonable outcome from an adaptiveevolutionary
standpoint (Rozin & Schull, 1988; Timberlake, 1983). The potential adaptiveness of excitatory backward conditioning is most obvious in the case of
noxious USs (e.g., Ayres, Haddad, & Albert, 1987; Razran, 1956, 1971). For
example, a prey animal that has been attacked by an unfamiliar predator may
improve its chances of avoiding similar future encounters if it learns something about the characteristics of the predator in the immediate aftermath of
the initial attack (Keith-Lucas & Guttman, 1975).
Excitatory backward conditioning also could be advantageous in situations
with an appetitive US, like food. Consider a frugivore that readily associates
cues present following consumption, such as the seeds or pits of palatable
fruit, with the fruit just eaten. Such cues could serve in the future as signals
for nearby fruit. An animal able to relate such backward cues to the proximity
of fruit without a series of forward pairings could be more efficient in foraging
than a conspecific that learned to approach such cues only after their repeated
forward pairings with eating.
A frequent difficulty with the intuitions of an adaptiveevolutionary viewpoint has been the problem of translating them into hypotheses that can be
tested within traditional learning paradigms. The behavior systems approach
(Timberlake & Fanselow, 1994; Timberlake & Lucas, 1989) incorporates
stimulus sensitivities and motor components into a framework that allows the
insights of the adaptiveevolutionary viewpoint to be tested and integrated
with traditional procedures and accounts of learning (Shettleworth, 1994; see
also Domjan, 1994; Fanselow, 1994; Hogan, 1994; Timberlake, 1994). In
addition to clarifying the contribution of system-typical organization to the
form of conditioned responding, the behavior systems approach postulates
a sequence of motivational modes (states) that precede and follow a US
(Timberlake & Lucas, 1989).
For example, food-finding behavior in a rat is assumed to involve a sequence of search and handling modes related to procuring and ingesting food
(Timberlake, 1986; Timberlake & Lucas, 1989; Timberlake & Silva, 1995).
In a typical sequence (illustrated in abstract form in Fig. 1), the rat is assumed
to begin in a general search mode characterized by attention to novel stimuli
and search for specific cues that better predict the location of food. When
better predictors of food are encountered, the animal enters a focal search
mode in which responses are more focused and related to the immediate
procurement of food. If food arrives, the focal search mode is followed by a
handling/consuming mode in which responses deal with handling and ingesting the food item. Following ingestion, the animal is assumed to again enter

AID

L&M 0928

/ ae01$$$$21

05-15-96 10:26:50

lmas

AP: L&M

132

SILVA, TIMBERLAKE, AND KOEHLER

FIG. 1. A representation of the sequence of search modes and the general response classes
related to procuring and ingesting food. The dashed line through the focal search mode is meant
to represent the asymmetric nature of pre- and postfood focal search.

a type of focal search mode (post food focal search; see also Krebs, 1973;
Whishaw & Gorny, 1991). If more food is rapidly encountered, the animal
re-enters a handling and consuming mode; otherwise it will return to a general
search mode and then either repeat the cycle or stop foraging (Timberlake &
Lucas, 1989; Timberlake & Silva, 1995).
In the behavior systems view, a CS can control behavior through two
related pathways: by evoking a search mode (thereby activating an organized
subset of stimulus sensitivities and response tendencies related to the US)
and by directly eliciting specific conditioned and unconditioned response

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

133

BIDIRECTIONAL EXCITATORY CONDITIONING

components related to the CS. The precise action of a CS will depend upon
the relation of its physical qualities to the sensory filters of specific perceptualmotor modules, and on how its spatial and temporal distance from the
US fit with the sequence of search modes characterizing foraging. In the case
of forward CSUS pairings in rats involving relatively nonspecific CSs,
more general search responses such as searching for and approaching distant
moving cues should emerge at longer CSUS intervals. More focal search
responses such as approaching the food site should emerge at short CSUS
intervals (e.g., Akins, Domjan, & Gutierrez, 1994).
Responding in backward conditioning also should be related to the species
foraging sequence. Responses appropriate to postfood focal search should
emerge with short backward intervals, but responses more related to the early
stages of general search should emerge with longer intervals. In the case of
rats in an experimental chamber, this would imply that responses like nosing
in the feeder should occur immediately after food, followed by area-restricted
search, and more widespread search at longer backward intervals. As we will
discuss later, there are several reasons to assume that conditioning should be
asymmetric with forward vs backward CSs. Backward CSs most likely evoke
search modes more than they directly condition specific responses (CRs), and
the temporal extent of these modes may differ from those associated with
forward CSs.
The purpose of the present research was to use a behavior systems framework to explore bidirectional excitatory conditioning under a common serial
conditioning procedure. A serial procedure was chosen because it allowed us
to differentiate the temporal stream of motivation and behavior preceding and
following delivery of the US and to examine its contribution to subsequent
conditioning. Rats were exposed initially to either three-element forward serial
CSUS pairings or backward serial USCS pairings (Experiment 1a). In
Experiment 1b, all rats received a compound conditioning manipulation in
which food was presented immediately following presentation of one of the
serial elements combined with a novel stimulus (a lever). Conditioned responding was measured in terms of percentage of trials nosing in the feeder
during serial training and in terms of nosing in the feeder and percentage of
trials with a lever contact during compound conditioning.
EXPERIMENT 1a: FORWARD AND BACKWARD
SERIAL CONDITIONING

From a behavior systems perspective, the temporal distance of a serial

element from the US should be predominately inversely correlated with the
strength of the focal search mode and directly correlated with the strength of
the general search mode conditioned to that element. That is, more temporally
proximal elements should be correlated with the conditioning of a stronger
focal search mode than more temporally remote elements; the latter should

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

134

SILVA, TIMBERLAKE, AND KOEHLER

be more related to the conditioning of a general search mode. This prediction

shares aspects of Konosrkis (1967) account that elements remote from the
US should control stronger preparatory CRs but more proximal elements
should control stronger consummatory CRs (although see Timberlake & Silva,
1995, for a discussion of the differences between Konorskis model and the
behavior systems framework).
The behavior systems view contrasts with the traditional associative view
that the ability of a CS to control behavior should fall along a unidimensional
strength of conditioning or inhibitionexcitation continuum. In the
behavior systems view, a short CSUS interval does not necessarily result
in a stronger CR than a long CSUS interval, nor do backward paired CSs
inevitably result in inhibition of responding. If we measure behavior primarily
related to a focal search mode, then maximum responding should occur at
shorter CSUS intervals; but, if we measure behavior primarily controlled
by a general search mode, then maximum responding should occur at longer
CSUS intervals (e.g., Akins et al., 1994).
Thus, in the behavior systems view, forward pairings of a serial CS with
food (FCSF FCSI FCSN Food, where the subscripts F, I, and N denote,
respectively, the elements Far, Intermediate, and Near to food) should produce
maximum nosing in the feeder (representing focal search) during the Near
serial-element, with successively less control of this response by the Intermediate and Far stimuli (FCSN FCSI FCSF). In contrast, the strength of a
general search mode and related responses should be the reverse (FCSF
FCSI FCSN). It is worth noting that we did not directly measure general
search responses in these experiments and that even the Far serial element
in our study is not sufficiently temporally distant from the US to acquire
control of a strong general search mode. However, relative to the other serial
elements, the Far element should come to control the strongest general search
mode and related behavior.
In backward serial conditioning (FoodBCSN BCSI BCSF), elements
more temporally proximal to food should condition a postfood focal search
mode more than elements farther away. The more distant elements should
better condition the early stages of general search. As a result, nosing in
the feeder during training should be highest in the initial stimulus element,
decreasing during the elements of the serial CS further from food (BCSN
BCSI BCSF).
Method
Subjects. The subjects were 48 female SpragueDawley (Rattus norvegicus) rats that were approximately 90 days old at the start of the experiment.
They were maintained at 85% of their free-feeding weights throughout the
course of the experiment, and they were housed in individual cages in a

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

135

colony room regulated by a 12-hr:12-hr light:dark cycle. Water was freely

available in the home cages.
Apparatus. The apparatus consisted of four metal rectangular boxes (50 1
36 1 32 cm) with a Plexiglas front and top. Each box was contained in a
sound-attenuating wood chamber and dimly illuminated by a 25-W light bulb
oriented toward the ceiling. A fan located at the back of each chamber provided masking noise and ventilation.
Food pellets (Bio Serv 45-mg dustless pellets, Frenchtown, NJ) were delivered by a Waltke Feeder (Bloomington, IN) into a metal food tray located in
a recessed opening on the back wall of the box. The feeder aperture was 19.5
cm from the right side wall, 15.0 cm from the left side wall, and 5 cm above
the floor. An infrared photodetector measured each time the subject placed
its head in the food tray. A touch-sensitive retractable lever was located on
the left side of the food receptacle, 4 cm from the feeder, 7 cm from the left
side wall, and 4.5 cm above the floor. A green jewel light (24-V DC) was
located 7 cm above the floor, 3.5 cm from the left of the feeder.
The apparatus was controlled by an IBM-PC and solid-state interface located in an adjacent room. Programmed contingencies and data collection
were managed at a 0.1-s resolution, using Conman Contingency Management
Software (Spyder Systems, Bloomington, IN).
Procedure. Twenty-four rats were used over a 4-week period, and another
24 rats were used over a subsequent 4-week period. Experimental sessions
occurred 6 days a week at approximately the same time each day. Rats were
weighed before each session, and, following the session, fed a supplemental
amount of food to maintain their weights at 85% ad lib. The rats were fed
at the same time on the 7th day. Within the 4-week period that they were
run, the order of groups was alternated each day to eliminate any time bias.
Each session consisted of 12 trials. The interfood interval (IFI) averaged 90
s, with a range between 60 and 120 s. The experiment preceded through the
following three stages: chamber adaptation, pretraining (feeder training), and
serial conditioning.
Before actual training took place, all rats were placed in the boxes for
approximately 20 min to reduce neophobia to the experimental environment.
Following this chamber adaptation phase, the rats were feeder trained by
placing them in the chambers for a 20-min session during which approximately 24 food pellets (i.e., 2 pellets per trial 1 12 trials) were delivered.
On the 2nd day, those rats that did not eat the food on the first day were
trained again using the same procedure as the 1st day.
The serial conditioning phase lasted 12 days. The 24 rats receiving forward
serial training were exposed to three 8-s elements followed by food; the 24
rats receiving backward serial training were treated similarly except that food
was delivered immediately before the onset of the first element in the serial
CS. The serial element was identified by a multiletter code. The first letter

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

136

SILVA, TIMBERLAKE, AND KOEHLER

identifies whether the elements were part of a forward (F) or backward (B)
serial CS; the subscript identifies the temporal proximity of an element to the
US (Far, Intermediate, Near; abbreviated F, I, or N, respectively). FCSF and
BCSN was a nonflashing light, FCSI and BCSI was a light that flashed at a
0.5-s on/off rate, and FCSN and BCSF was a light that flashed at a 0.1-s on/
off rate. Table 1 shows a summary of the experimental procedures and the
groups, including the compound conditioning phase described below as part
of Experiment 1b.
Data analysis. Statistical significance was determined at p .05 for all
analyses. The results from forward and backward training are presented together for the purposes of exposition; however, because of space and time
limitations, the two types of training were conducted sequentially, and so
were analyzed separately. There were some sessions during backward conditioning in which feeder entries were not accurately counted in one experimental chamber; therefore, the data from these chambers on those days were
excluded from the relevant analyses. It may be because of this loss of statistical
power that some seemingly large differences in nosing in the feeder were not
statistically significant (see below).
Results and Discussion
Figure 2 (left) shows a progressive increase in the percentage of trials spent
nosing in the feeder across elements for the rats that received forward serial
conditioning. An analysis of variance (ANOVA) across 2-day blocks showed
main effects of element [F(2,46) 67.86] and days [F(5,115) 6.05] and
an interaction between element and days [F(10,230) 12.09]. Fishers least
significant difference (lsd) test confirmed that nosing in the feeder differed
between all pairs of elements.
Figure 2 (right) shows a progressive decrease in the percentage of trials
spent nosing in the feeder across elements for the rats that received backward
serial conditioning. An ANOVA across 2-day blocks showed main effects of
element [F(2,34) 186.94] and days [F(5,21) 5.41] and an interaction
between element and days [F(5,85) 37.53]. An lsd test confirmed that
nosing in the feeder differed between all pairs of elements.
The results during forward conditioning showed that nosing in the feeder
during the serial CS increased as the distance of the serial element from
food decreased (i.e., FCSF FCSI FCSN). In contrast, during backward
conditioning, nosing in the feeder decreased markedly from the Near to the
Intermediate and Far elements of the serial CS (i.e., BCSN BCSI BCSF).
Conceptually, the direct relation between nosing in the feeder and the
proximity of the forward serial element to food readily supports both the
behavior systems and the traditional associative views. The behavior systems
view presumes that the more proximal elements of a forward serial CS control
a stronger focal search mode and focal CR than more remote elements. Ac-

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

137

BIDIRECTIONAL EXCITATORY CONDITIONING

TABLE 1
Design Summary for Experiments 1a and 1b
Experiment 1a: Serial conditioning
Subjects

Stimulus presentations

24 Rats
24 Rats

12 FCS (F)FCS (I)FCS (N) food

12 foodBCS(N)BCS(I)BCS(F)
Experiment 1b: Compound conditioning

Subjects
(8 Rats/Group)

Stimulus presentations

Group FCS(F)
Group FCS(I)
Group FCS(N)

10 FCS(F)/leverfood/2 leverfood
10 FCS(I)/leverfood/2 leverfood
10 FCS(N)/leverfood/2 leverfood

Group FCS(F)
Group FCS(I)
Group FCS(N)

10 BCS(N)/leverfood/2 leverfood
10 BCS(I)/leverfood/2 leverfood
10 BCS(F)/leverfood/2 leverfood

Note. Numbers represent the number of each type of trial given each day.

cording to an associative account of forward serial conditioning, each element

of a serial CS acquires its own associative strength in direct relation to its
temporal proximity to the US. The strongest CR appears during the element
closest to the US, and elements remote from the US control weaker and
possibly inhibitory CRs (Kehoe & Napier, 1991).
In contrast, the results of the backward serial conditioning procedure were
most consistent with the behavior systems view that temporally proximal
elements immediately following food should control a stronger postfood focal
search mode than more temporally remote elements. According to a traditional
associative account of backward serial conditioning, each element should
control inhibitory associations. Thus, the slow decline of nosing in the feeder
during the Intermediate and Far elements may be due to the progressive
inhibition of this response, though it is unclear which responses, if any, the
Near element inhibited.
EXPERIMENT 1b: COMPOUND CONDITIONING

In Experiment 1b, the rats used in the forward and backward procedures
of Experiment 1a were divided into groups and presented with one of the
serial elements conditioned in Experiment 1a compounded with presentation
of a novel stimulus (a lever) and followed by food. This procedure allowed
us to further examine the behavior systems view that the serial elements

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

138

SILVA, TIMBERLAKE, AND KOEHLER

FIG. 2. Percentage of trials in which all rats nosed in the feeder during the serial forward (left)
and backward (right) conditioning phase.

conditioned in Experiment 1a differentially controlled types of search modes.

It also allowed further comparison of this view with a more traditional associative account.
The behavior systems view predicts that following forward serial conditioning, the serial elements closer to food should differentially control search
modes and responses closest to feeding (e.g., focal search and nosing in the
feeder). In contrast, elements farther from food should more readily support
responses related to a late general search mode. Thus, in a predatory animal
like the rat, presentation of a moving stimulus such as a lever should more
readily trigger approach and manipulation when combined with a more distal
serial element than when combined with a more proximal serial element
(Timberlake, Wahl, & King, 1981). Not only should the proximal serial
element control a less compatible search mode, it also should control specific
responses that compete for expression with lever-directed behavior. In terms
of the amount of lever-directed behavior, this implies a response ordering in
the initial compound trials of FCSF FCSI FCSN .
Following backward serial conditioning, the behavior systems view predicts
that serial elements closer to food should have stronger control of a postfood
focal search mode than elements farther away. The latter elements should
better control the early stages of general search. However, in the case of
backward conditioning, there should be less significant competition with CRs.
In addition, the postfood focal search mode should facilitate behavior directed
toward the lever (the movement of which mimics some characteristics of prey
item) better than an early general search mode. This implies a response
ordering in the initial compound trials of BCSN BCSI BCSF .
A traditional associative account of the effects of compound training on
rats that previously received forward serial conditioning makes predictions
similar to those of the behavior systems view. Competition from associative

AID

L&M 0928

/ ae01$$$$22

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

139

links or from the response of nosing in the feeder should decrease with
distance of the serial element from food in the original training. Thus, maximal
lever contact should occur during the most distal element where there is the
least competition based on prior conditioning.
An associative account of the effects of backward serial conditioning is
more complicated. Most associative accounts predict that the serial elements
should control inhibitory associations because the CS predicts the absence of
biologically important events (Hollis, 1982; Mackintosh, 1983; Miller &
Spear, 1985; although see Hearst, 1989; Larew, 1986; Tait & Saladin, 1986).
If the maximum inhibitory strength were in the Intermediate and Far elements
(Wagner, 1981; Wagner & Brandon, 1989), then initial responding to the
lever should be lowest in compounds with these elements. For all elements,
though, we would expect lower levels of responding than for the rats that
received forward serial conditioning. Alternatively, if backward serial conditioning produced excitatory conditioning that was reflected in the level of
nosing in the feeder shown in Experiment 1a, then competition with conditioned nosing in the feeder or with the associations underlying it should
produce the least initial lever contact for the most proximal serial element.
Method
Subjects. The rats that participated in Experiment 1a served in Experiment
1b. The animals were maintained as in Experiment 1a.
Apparatus and procedures. The apparatus was the same as in Experiment
1a. The 24 rats previously exposed to forward serial conditioning were divided
into three groups of eight, equated for their ad lib weights. The 24 rats exposed
to backward serial conditioning were similarly divided. The compound conditioning phase directly followed the serial conditioning phase and also lasted
12 days. In the compound conditioning phase, one of each of the groups
received one of the serial elements in compound with insertion of the lever.
The multiletter code used above identified the group. Thus, Groups FCSF and
BCSN received the nonflashing light simultaneously with the lever, Groups
FCSI and BCSI received the light that flashed at a 0.5-s on/off rate in compound with the lever, and Groups FCSN and BCSF received the light that
flashed at a 0.1-s on/off rate in compound with the lever. The lightlever
compound stimulus was presented for 8 s for all groups, and food was delivered simultaneously with the offset of the stimulus. The lever was presented
alone for two of the 12 trials in a given day to serve as a probe of lever
responding in the absence of mediation by the serial element. Food followed
all stimulus presentations.
Results
The left graph of the top panel in Fig. 3 shows the percentage of trials
with a lever contact during the compound conditioning phase for the rats that

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

140

SILVA, TIMBERLAKE, AND KOEHLER

previously received forward serial conditioning. There appears to be an increase in contact across days. Group FCSF showed the most contacts, followed
by Groups FCSI and FCSN , the latter of which showed the least amount of
contacts. An ANOVA across 2-day blocks showed no main effect of group
[F(2,21) .69], but did show a main effect of days [F(5,105) 15.39] and
an interaction between group and days [F(10,105) 2.13]. An lsd test confirmed that all groups differed from each other during the first 2-day block.
The mean percentage trials, averaged across all days, in which the rats contacted the lever when it was compounded with the serial element vs when
the lever was presented alone was 82.3 and 86.0, respectively. An ANOVA
conducted across 2-day blocks and trial-type (compound vs. lever-alone)
showed no main effect of group [F(2,21) .80], but main effects of days
and trial-type [F(1,21) 4.64, F(5,105) 10.33, respectively]. There were
no significant interactions.
The right graph of the top panel in Fig. 3 shows the percentage of trials
with a lever contact during the compound conditioning phase for the rats that
previously received backward serial conditioning. There appears to be an
increase in contact across days. Groups BCSN and BCSI showed the most
contacts, and Group BCSF showed the fewest contacts. An ANOVA across
2-day blocks showed a main effect of group [F(2,21) 3.55] and days
[F(5,105) 10.35]. An lsd test confirmed that Group BCSN differed from
Group BCSF , which marginally differed from Group BCSI (p .06) during
the first 2-day block. The mean percentage trials in which the rats contacted
the lever during compound and lever-alone trials averaged across all days was
82.08 and 80.25, respectively. An ANOVA conducted across 2-day blocks and
trial-type (compound vs lever-alone) showed only a main effect of days
[F(5,75) 3.49].
The left graph of the bottom panel in Fig. 3 shows the percentage of
trials in which the rats nosed in the feeder during the compound conditioning phase for the rats that previously received forward serial conditioning.
An ANOVA across 2-day blocks showed only a main effect of days
[F(5,105) 6.95]. However, an lsd test applied only to the data of the first
2-day block of trials showed that Group FCSN nosed in the feeder significantly more than Group FCSF . The mean percentage trials in which the
rats nosed in the feeder during compound and lever-alone trials averaged
across all days was 81.82 and 75.52, respectively. An ANOVA conducted
across 2-day blocks and trial-type showed no main effect of group [F(2,21)
2.20], but main effects of days and trial-type [F(1,21) 9.09, F(5,105)
11.86, respectively]. There was also a significant interaction between
trial-type and days [F(5,105) 3.72].
The right graph of the bottom panel in Fig. 3 shows the percentage of trials
in which the rats nosed in the feeder during the compound conditioning
phase for the rats that previously received backward serial conditioning. There

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

141

FIG. 3. (Top) Percentage of trials with a lever contact when the lever was compounded with
one of the elements from the forward (left) or backward (right) serial CS. (Bottom) Percentage
of trials with an instance of nosing in the feeder when the lever was compounded with one of
the elements from the forward (left) or backward (right) serial CS.

appear to be no differences among groups. An ANOVA across 2-day blocks

showed only a main effect of days [F(5,75) 5.41]. An lsd test applied only
to the first 2-day block of trials found no significant differences between
groups. The mean percentages of trials in which the rats nosed in the feeder
during compound and lever-alone trials averaged across all days were 68.4
and 69.1, respectively. An ANOVA conducted across 2-day blocks and trialtype showed only a main effect of days [F(5,105) 7.57].
Discussion
When each element of the forward serial CS was presented individually
with a novel lever and followed by food, Group FCSF initially contacted the
lever significantly more than Groups FCSI and FCSN and nosed in the feeder
less than Group FCSN . However, differences in lever contact and nosing in

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

142

SILVA, TIMBERLAKE, AND KOEHLER

the feeder waned as compound trials continued. Further, lever-alone trials

during the compound condition produced significantly more lever contact and
less nosing in the feeder than compound trials, suggesting competition for
expression between contacting the lever and nosing in the feeder. In general,
these results fit both the behavior systems view and a traditional associative
account.
When each element of the backward serial CS was presented individually
with a novel lever and followed by food, Groups BCSN and BCSI contacted
the lever more than Group BCSF . These data failed to show any evidence of
competition between backward conditioning and subsequent forward compound conditioning. There was no inverse relation between nosing in the
feeder during the serial CS and the subsequent levels of lever contact in
compound conditioning. For example, Group BCSN showed the highest
amount of both nosing in the feeder and contacting the lever in the initial
compound trials. Also, there were no differences between lever-alone and
compound trials during Experiment 1b.
These results are most consistent with the behavior systems hypothesis that
temporally proximal elements are correlated with a stronger postfood focal
search mode than more temporally remote elements. When compounded with
a novel moving cue, elements evoking a strong postfood focal search mode
(e.g., Groups BCSN and BCSI) facilitated responding to the moving stimulus.
A moving cue, such as a lever proximal to food, should support handling,
biting, and tuggingresponses consistent with postfood focal search (Timberlake & Lucas, 1989).
GENERAL DISCUSSION

This research explored forward and backward excitatory serial conditioning

within a behavior systems framework. In the acquisition phase of Experiment
1a, rats were exposed to either a forward serial CS (FCSF FCSI FCSN
Food) or a backward serial CS (FoodBCSN BCSI BCSF) consisting of
8-s elements. During the subsequent forward compound condition in Experiment 1b, different subgroups of rats received one of the serial elements
compounded with a novel lever. This compound stimulus was always followed
by food.
The primary result was evidence for bidirectional (both forward and backward) excitatory conditioning with an asymmetrical temporal distribution
around the US. During forward serial training, nosing in the feeder during
the elements of the serial CS was directly related to the proximity of the
element to food. The greatest responding occurred during the Near element,
and the least responding occurred during the Far element. During backward
serial training, nosing in the feeder was also highest in the Near element and
lowest in the Far element. However, in partial contrast to the forward case,
nosing in the feeder was low during the Intermediate element.

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

143

The apparent asymmetry of control by the serial elements was even more
compelling during compound conditioning. When, following forward serial
training, presentation of the Far, Intermediate, and Near elements from Experiment 1a were combined (singly) with a novel lever in forward pairings, FCSF
supported the most lever contact during the first block of trials. In contrast,
following backward serial training, the forward compound of BCSF with the
novel lever produced the least lever contact. The most lever-directed behavior
occurred in the presence of the BCSN and BCSI elements.
A second finding of these experiments was that there was evidence of
competition for expression between nosing in the feeder and contacting the
lever following forward serial training, but not backward training. During
compound conditioning, there was more lever contact during the lever-alone
trials than during the compound trials following forward serial training, an
effect absent from the results following the backward procedure. Further,
there was an inverse relation between nosing in the feeder during acquisition
and lever contact during the compound condition for the forward conditioned
animals, but there was a direct relation between these CRs for the backward
conditioned animals. A ready interpretation of these results was that specific
responses were less strongly conditioned in the backward case than in the
forward.
It is worth noting that in comparing forward and backward serial conditioning procedures it is necessary to confound either the order of the serial
elements or the proximity of individual elements to the US with the backward
vs forward manipulation, or to mix confounds within forward or backward
procedures. We chose to confound the proximity of the serial element to food
with the forward vs backward manipulation, thus preserving the same coherent
sequence of cues for all animals (first a steady light, then a flashing light,
then a faster flashing light). Our choice meant that the same serial element
was the Far element in the forward CS and the Near element in the backward
CS. This makes it possible to argue that the amount of lever contact was due
to the sequence of serial elements (i.e., the greatest lever contact occurred in
the initial trials of compound conditioning with the steady light, and the least
lever contact occurred with the most rapidly flashing light).
For numerous reasons, though, this is an unlikely account. First, if the
specific serial sequence were the major determinant of the results, we would
have expected the same pattern of lever contacting over the sequence of
elements following forward and backward serial conditioning. An obvious
exception is that the Intermediate serial element supported relatively low
lever contact following forward conditioning, but relatively high lever contact
following backward conditioning (see Fig. 3). Second, if the sequence of
serial elements were the critical determinant, then the results for nosing in
the feeder during serial conditioning should show similar patterns for forward
and backward conditioning. However, the pattern for nosing in the feeder

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

144

SILVA, TIMBERLAKE, AND KOEHLER

appears to contradict control by the particular sequence of elements, showing

more symmetry around the US. Third, subsequent experiments conducted in
our lab have confounded both the order of serial elements and their temporal
proximity with the backward vs forward manipulation by randomizing the
order of elements. This procedure has shown results compatible with those
of the present experiments. Together these issues question the specific sequence of serial elements as a major determinant of the present results.
Theoretical Accounts
The behavior systems account. The present evidence of bidirectional excitatory conditioning is compatible with a behavior systems view of food-related
learning during Pavlovian procedures (see Timberlake, 1994). In the behavior
systems view, a hungry animal begins a feeding sequence in a general search
mode, characterized by attention to novel cues and the search for better
predictors of food. When a sufficiently better predictor occurs, the animal
moves into a focal search mode in which responses are related to the immediate procurement of food. The focal search mode is followed by a handling/
consuming mode in which responses consist of handling and ingesting a food
item. Following food the animal is assumed to enter a postfood focal search
mode (Lucas et al., 1988), either to return to handling/consuming if a strong
predictor of food (or food itself) is shortly encountered or to continue to a
more general search mode in the absence of further local search cues (Timberlake & Lucas, 1989; Timberlake & Silva, 1995).
Forward conditioning involves the pairing of cues temporally related to
this sequence with the presentation of the US anchoring one end of a feeding
sequence. Thus, during serial training, the conditioning of a focal search mode
and the related response of nosing in the feeder increased across elements of
the serial CS to reach a maximum during the serial element closest to food.
In contrast, the conditioning of a general search mode and any appropriate
search behaviors was assumed to be greatest with the Far element and decline
in the elements closer to food.
During initial compound conditioning with the lever, the Far serial element
(FCSF) was predicted to show the most control of lever-directed behavior
because it presumably supported the general search mode the most of the
three serial-elements. The general search mode was presumed to facilitate
interactions with the lever. In contrast, during backward serial conditioning
the US anchors the beginning of the sequence of post food search. The
proximal elements of the CS should control aspects of search behavior selected
for their likelihood in finding other food. One such aspect is a sensitivity to
prey or stimuli that mimic some characteristics of prey (e.g., sound, movement). Thus, maximal contact of a spatially proximal lever should occur when
it is compounded with a stimulus controlling a postfood focal search mode.

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

145

More distal elements should come to control the early stages of a general
search mode, which should be less sensitive to proximal prey stimuli.
These data combine with others (e.g., Timberlake & Lucas, 1991) to suggest
that pre- and postfood focal search are related but not identical, and that their
differences may contribute to the lack of similarity between forward and
backward conditioning. At an empirical level, the data suggest that postfood
focal search lasts a shorter time than the prefood focal mode. Thus, nosing
in the feeder decreases more rapidly as a function of the interval between a
serial element and the US in backward conditioning than in forward conditioning. Also, during compound conditioning, lever-directed behavior was supported by serial elements temporally closer to the US in the backward than
in the forward case.
On the other hand, the relatedness of pre- and postfood focal search was
evident in the high levels of lever contact in the initial trials of compound
conditioning when the lever was combined with the BCSN or BCSI elements.
If the postfood search mode were not compatible in some respects with
prefood focal search, lever-directed responding should not have readily occurred in compound conditioning. Instead, backward conditioning should have
interfered with contacting the lever.
Another difference between forward and backward conditioning is that
backward paired CSs primarily appear to control search modes but forward
paired CSs control both search modes and specific responses. First, in backward conditioning, there are no instrumental or higher-order Pavlovian contingencies to support specific responses. Responding after the US is not followed
by imminent food nor a predictive cue that can function like a conditioned
reinforcer or a higher-order CS. Backward pairings probably are sufficient to
condition search modes because of their preorganized sequence, but individual
responses are not as fixed in order (see Timberlake, 1994; Timberlake &
Lucas, 1989; Timberlake & Silva, 1995). Thus, backward paired CSs may
come to evoke a postfood focal search mode more readily than they directly
elicit particular responses. Compatible with this view is the surmise that the
postfood search mode may include a set of response tendencies elicited by
finding food that have evolved to increase the probability of finding more
food (see Timberlake & Lucas, 1991; Whishaw & Gorny, 1991). These responses include a sensitivity to prey items or moving stimuli that mimic some
characteristics of prey. Finally, it follows from these ideas that there should
be less competition between alternative CRs when a backward cue is made
a stronger predictor.
The traditional associative account. Although the results from both experiments are consistent with a behavior systems account, several aspects of the
results are also consistent with more traditional associative explanations (e.g.,
Gormezano & Kehoe, 1989; Kehoe, 1982). According to an associative account of forward serial conditioning, each element of a serial CS acquires its

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

146

SILVA, TIMBERLAKE, AND KOEHLER

own associative strength in direct relation to its temporal proximity to the

US. The strongest CR appears during the element closest to the US, and
elements remote from the US control weaker and possibly inhibitory CRs
(Kehoe & Napier, 1991). This account explains the direct relation between
nosing in the feeder and the proximity of the serial element to the US in
initial training. In compound conditioning, when an element of the serial CS
was presented in compound with a lever, a blocking explanation could predict
that the strongest elicitor (FCSN) should block responding to the lever more
than the weakest elicitor (FCSF).
In backward conditioning, it is customary to invoke the concept of inhibition to explain the negative effects of backward CSs on subsequent conditioning (e.g., Hall, 1984). In the present case, inhibition could be inferred on the
basis of the decrease in nosing in the feeder during elements BCSI and BCSF
during serial training, but this would not explain the rapid conditioning of
lever-directed responding for Group BCSI during the compound condition.
In the absence of further tests, it might be argued that the BCSI serial element
acquired inhibitory properties during initial training, which resulted in superconditioning during compound conditioning (Rescorla & Wagner, 1972).
However, this would not by itself explain why Group BCSN showed even
better conditioning during the compound procedure in the absence of any
evidence of inhibition in previous backward training.
Perhaps most importantly, there is no indication of inhibition of either
lever contact or nosing in the feeder relative to the levels shown in the
forward conditioning case during the initial compound trials. If inhibition
played an important role in the results of backward conditioning, one
would expect to find these levels well below the amount shown by the
forward groups. We do not intend to argue here that inhibition did not
contribute to the present results, only that it alone cannot account for the
data patterns.
Toward integration. It seems clear that both forward and backward pairing of
stimuli result in the acquisition of some form of associations among stimuli,
aspects of related responses, and the outcome. However, the traditional associative
approach has several drawbacks as a general account of the evidence for asymmetrical excitatory conditioning in forward and backward procedures. For example, purely associative concepts such as blocking or inhibition are clearest when
their analysis is restricted to a single CR (Timberlake & Silva, 1994). Such a
restriction, though, may be inappropriate given the occurrence of multiple CRs
in many circumstances, including instances of signal- and goal-directed behavior
(Boakes, 1977; Brown et al., 1993; Brown & Jenkins, 1968; Davey & Cleland,
1982; Hearst & Jenkins, 1974; Silva, Silva, & Pear, 1992). The behavior systems
approach provides a framework clarifying the nature of the conditioning and
how responding is controlled and should be measured (Timberlake & Silva,
1994). Issues such as the temporal course of conditioning, the effect of compound-

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

147

ing serial elements with a moving stimulus, and the existence of response competition in the forward but not the backward paradigms all are compatible with
placing the conditioning of associations within a behavior systems framework
(Timberlake, 1994). Neither the behavior systems view nor the present experiments rule out the role of associative variables (see also Suboski, 1990; Timberlake, 1994).
The results for backward conditioning in particular argue that a behavior
systems framework may be able to meld adaptiveevolutionary and associative concerns into a single approach (Timberlake, 1994). The present data
provide support for and constraints on the adaptiveevolutionary speculation
that animals could profit from backward excitatory conditioning involving
food. Backward conditioning of a postfood focal search mode appears to
evoke a search mode that under natural conditions could increase the likelihood of finding food. In the rat, behaviors related to postfood focal search
consist of searching in the immediate vicinity of found food and approaching
and contacting moving stimuli near that location.
Finally, the behavior systems approach predicts the form of CRs by arguing
that responding should follow a natural foraging sequence (Timberlake &
Silva, 1995). The animal should engage in the most appropriate responses
from its repertoire based on the physical characteristics of the CS and US
and their spatial and temporal arrangement. In this view, a reduction in responding due to compounding stimuli is not inevitably the result of an associative deficit (see also Brown, Hemmes, Cabeza de Vaca, & Pagano, 1993),
but the outcome of interactions among different search modes or competition
within them (Timberlake, 1986).
REFERENCES
Akins, C. K., Domjan, M., & Gutierrez, G. (1994). Topography of sexually conditioned behavior
in male Japanese quail (Coturnix japonica) depends on the CS-US interval. Journal of
Experimental Psychology: Animal Behavior Processes, 20, 199209.
Ayres, J. J. B., Haddad, C., & Albert, M. (1987). One-trial excitatory backward conditioning as
assessed by conditioned suppression of licking in rats: Concurrent observations of lick
suppression and defensive behaviors. Animal Learning & Behavior, 15, 212217.
Boakes, R. A. (1977). Performance on learning to associate a stimulus with positive reinforcement. In H. Davis & H. M. B. Hurwitz (Eds.), OperantPavlovian interactions (pp. 67
97). Hillsdale, NJ: Erlbaum.
Brown, B. L., Hemmes, N. S., Cabeza de Vaca, S., & Pagano, C. (1993). Sign- and goal-tracking
during delay and trace autoshaping in pigeons. Animal Learning & Behavior, 21, 360368.
Brown, P. L., & Jenkins, H. M. (1968). Autoshaping of the pigeons key peck. Journal of the
Experimental Analysis of Behavior, 11, 18.
Davey, G. C. L., & Cleland, G. G. (1982). The effect of partial reinforcement on the acquisition
and extinction of sign-tracking and goal-tracking in the rat. Bulletin of the Psychonomic
Society, 19, 115118.
Domjan, M. (1994). Formation of a behavior system for sexual conditioning. Psychonomic
Bulletin & Review, 1, 421428.

AID

L&M 0928

/ ae01$$$$23

05-15-96 10:26:50

lmas

AP: L&M

148

SILVA, TIMBERLAKE, AND KOEHLER

Fanselow, M. S. (1994). Neural organization of the defensive behavior system responsible for
fear. Psychonomic Bulletin & Review, 1, 429438.
Gormezano, I., & Kehoe, E. J. (1989). Classical conditioning with serial compound stimuli. In
J. B. Sidowski (Ed.), Conditioning, cognition, and methodology: Contemporary issues in
experimental psychology. Lanham, MD: Univ. Press of America.
Hall, J. F. (1984). Backward conditioning in Pavlovian type studies: Reevaluation and present
status. Pavlovian Journal of Biological Science, 19, 163169.
Hearst, E. (1989). Backward associations: Differential learning about stimuli that follow the
presence versus the absence of food in pigeons. Animal Learning & Behavior, 17, 280
290.
Hearst, E., & Jenkins, H. M. (1974). Sign tracking: The stimulusreinforcer relation and direct
action. Austin, TX: Monograph of the Psychonomic Society.
Hemmes, N. S., Brown, B. L., & Cabeza de Vaca, S. (1994). Appetitive backward conditioning
in pigeons. The Psychological Record, 44, 221237.
Hogan, J. A. (1994). Structure and development of behavior systems. Psychonomic Bulletin &
Review, 1, 439450.
Holland, P. C. (1984). Origins of behavior in Pavlovian conditioning. In G. H. Bower (Ed.), The
psychology of learning and motivation (Vol. 18, pp. 129174). Orlando, FL: Academic
Press.
Hollis, K. L. (1982). Pavlovian conditioning of signal-directed action patterns and autonomic
behavior: A biological analysis of function. Advances in the Study of Behavior, 12, 164.
Kehoe, E. J. (1982). Conditioning with serial compound stimuli: Theoretical and empirical issues.
Experimental Animal Behaviour, 1, 3165.
Kehoe, E. J., & Napier, R. M. (1991). Real-time factors in the rabbits nictitating membrane
response to pulsed and serial conditioned stimuli. Animal Learning & Behavior, 19, 195
206.
Keith-Lucas, T., & Guttman, N. (1975). Robust-single-trial delayed backward conditioning.
Journal of Comparative and Physiological Psychology, 88, 468476.
Konorski, J. (1967). Integrative activity of the brain. Chicago: Univ. of Chicago Press.
Krebs, J. R. (1973). Behavioral aspects of predation. In P. P. G. Bateson & P. H. Klopfer (Eds.),
Perspectives in ethology (pp. 73111). New York: Plenum.
Larew, M. B. (1986). Inhibitory learning in Pavlovian backward conditioning procedures involving a small number of USCS trials. Unpublished doctoral dissertation, Yale Univ.
Lucas, G. A., Timberlake, W., & Gawley, D. J. (1988). Adjunctive behavior of the rat under
periodic food delivery in a 24-hour environment. Animal Learning & Behavior, 16, 1930.
Mackintosh, N. J. (1983). Conditioning and associative learning. Oxford: Oxford Univ. Press.
Matzel, L. D., Held, F. P., & Miller, R. R. (1988). Information and expression of simultaneous
and backward associations: Implications for contiguity theory. Learning and Motivation,
19, 317344.
Miller, R. R., & Barnet, R. C. (1993). The role of time in elementary associations. Current
Directions in Psychological Science, 2, 106111.
Miller, R. R., & Matzel, L. D. (1989). Contingency and relative associative strength. In S. B.
Klein & R. R. Mowrer (Eds.), Contemporary learning theories: Pavlovian conditioning and
the status of traditional learning theory (pp. 6184). Hillsdale, NJ: Erlbaum.
Miller, R. R., & Spear, N. E. (Eds.) (1985). Information processing in animals: Conditioned
inhibition. Hillsdale, NJ: Erlbaum.
Pavlov, I. (1932). The reply of a physiologist to psychologists. Psychological Review, 39, 91
127.
Razran, G. (1956). Backward conditioning. Psychological Bulletin, 53, 5569.
Razran, G. (1971). Mind in evolution: An East-West synthesis of learned behavior and cognition.
Boston: HoughtonMiffin.

AID

L&M 0928

/ ae01$$$$24

05-15-96 10:26:50

lmas

AP: L&M

BIDIRECTIONAL EXCITATORY CONDITIONING

149

Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the
effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. G. Prokasy
(Eds.), Classical conditioning. II. Current research and theory (pp. 6499). New York:
AppletonCenturyCrofts.
Rozin, P., & Schull, J. (1988). The adaptiveevolutionary point of view in experimental psychology. In R. C. Atkinson, R. J. Herrnstein, G. Lindzey, & R. D. Luce (Eds.), Stephens
handbook of experimental psychology: Learning and cognition (2nd ed., Vol. 2, pp. 503
546). New York: Wiley.
Shettleworth, S. J. (1994). Commentary: What are behavior systems and what use are they?
Psychonomic Bulletin & Review, 1, 451456.
Silva, F. J., Silva, K. M., & Pear, J. J. (1992). Sign- versus goal-tracking: Effects of conditionedstimulus-to-unconditioned-stimulus distance. Journal of the Experimental Analysis of Behavior, 57, 1731.
Spetch, M. L., Wilkie, D. M., & Pinel, J. P. J. (1981). Backward conditioning: A reevaluation
of the empirical evidence. Psychological Bulletin, 89, 163175.
Suboski, M. D. (1990). Releaser-induced recognition learning. Psychological Review, 97, 271
284.
Tait, R. W., & Saladin, M. E. (1986). Concurrent development of excitatory and inhibitory
associations during backward conditioning. Animal Learning & Behavior, 14, 133137.
Timberlake, W. (1983). The functional organization of appetitive behavior: Behavior systems
and learning. In M. D. Zeiler & P. Harzem (Eds.), Advances in analysis of behavior:
Biological factors in learning (Vol. 3 pp. 177221). Chichester, England: Wiley.
Timberlake, W. (1986). Unpredicted food produces a mode of behavior that affects rats subsequent reactions to a conditioned stimulus: A behavior-system approach to context blocking.
Animal Learning & Behavior, 14, 276286.
Timberlake, W. (1994). Behavior systems, associationism, and Pavlovian conditioning. Psychonomic Bulletin & Review, 1, 405420.
Timberlake, W., & Fanselow, M. S. (1994). Symposium on behavior systems: Learning, neurophysiology, and development. Psychonomic Bulletin & Review, 1, 403404.
Timberlake, W., & Lucas, G. A. (1989). Behavior systems and learning: From misbehavior to
general principles. In S. B. Klein & R. R. Mowrer (Eds.), Contemporary learning theories:
Instrumental conditioning theory and the impact of biological constraints on learning (pp.
237275). Hillsdale, NJ: Erlbaum.
Timberlake, W., & Lucas, G. A. (1991). Periodic water, interwater interval, and adjunctive
behavior in a 24-hour multiresponse environment. Animal Learning & Behavior, 19, 369
380.
Timberlake, W., & Silva, F. J. (1994). Observation of behavior, inference of function, and the
study of learning. Psychonomic Bulletin & Review, 1, 7388.
Timberlake, W., & Silva, K. M. (1995). Appetitive behavior in ethology, psychology, and
behavior systems. In N. Thompson (Ed.), Perspectives in ethology (pp. 212254). New
York: Plenum.
Timberlake, W., Wahl, G., & King, D. (1981). Stimulus and response contingencies in the
misbehavior of rats. Journal of Experimental Psychology: Animal Behavior Processes, 8,
6285.
Wagner, A. R. (1981). SOP: A model of automatic memory processing in animal behavior. In
N. E. Spear & R. R. Miller (Eds.), Information processing in animals: Memory mechanisms
(pp. 547). Hillsdale, NJ: Erlbaum.
Wagner, A. R., & Brandon, S. E. (1989). Evolution of a structured connectionist model of
Pavlovian conditioning (AESOP). In S. B. Klein & R. R. Mowrer (Eds.), Contemporary
learning theories: Pavlovian conditioning and the status of traditional learning theory (pp.
149189). Hillsdale, NJ: Erlbaum.

AID

L&M 0928

/ ae01$$$$24

05-15-96 10:26:50

lmas

AP: L&M

150

SILVA, TIMBERLAKE, AND KOEHLER

Wagner, A. R., & Terry, W. S. (1975). Backward conditioning to a CS following an expected

vs. a surprising UCS. Animal Learning & Behavior, 3, 370374.
Whishaw, I. A., & Gorny, B. P. (1991). Postprandial scanning by the rat (Rattus norvegicus):
The importance of eating time and an application of warm-up movements. Journal of
Comparative Psychology, 105, 3944.
Received January 20, 1995
Revised June 20, 1995

AID

L&M 0928

/ ae01$$$$24

05-15-96 10:26:50

lmas

AP: L&M