Behavioural Processes 44 (1998) 147 – 162

Time as content in Pavlovian conditioning

Hernán I. Savastano, Ralph R. Miller *

Department of Psychology, SUNY-Binghamton, Binghamton, NY 13902 -6000, USA

Received 30 April 1998; received in revised form 7 August 1998; accepted 28 August 1998

Abstract

Time has played only a limited role within the traditional theories of Pavlovian conditioning. Although temporal
factors certainly contribute to whether conditioning occurs, the traditional assumption in the associative framework
has been that associations lack temporal information. Recently, the temporal coding hypothesis has challenged that
view, arguing that animals encode temporal relationships as part of associations. That is, proximal temporal
relationships not only foster associative learning, but also are part of the content of learning. The present paper
reviews for the nonspecialist the increasing empirical evidence that temporal coding is ubiquitous in Pavlovian
paradigms, including simultaneous and backward conditioning, second-order conditioning, sensory preconditioning,
cue competition, Hall–Pearce type CS-preexposure, and conditioned inhibition. The data support the temporal
coding hypothesis’ view that contiguity is sufficient for associative learning to occur, but challenge the central
assumption of the informational hypothesis that predictive relations are necessary for learning to occur (as opposed to
predictive relationships only being necessary for the expression of knowledge). © 1998 Elsevier Science B.V. All rights
reserved.

Keywords: Conditioned stimulus; Unconditioned stimulus; Time

1. Introduction depend critically on the temporal duration of

Time is inextricably tied to the study of Pavlo-
vian conditioning. In Pavlovian conditioning, or-
ganisms are said to form associations between
stimulus events that occupy temporal space. Suc-
cessful conditioning has long been recognized to
* Corresponding author. Tel: + 1 607 7772291/7987632;
fax: + 1 607 7774890/2607; e-mail: rmiller@binghamton.edu
those events as well as on their temporal relation-
ship (Pavlov, 1927). For example, some degree of
proximity in time (and space, but this article is
concerned exclusively with time) must clearly exist
between two stimulus events in order for those
events (or, more precisely, their representations)
to become associated. Yet, despite the consider-
able importance of temporal variables in Pavlo-
vian conditioning, time has played a surprisingly

0376-6357/98/$ - see front matter © 1998 Elsevier Science B.V. All rights reserved.
PII: S0376-6357(98)00046-1
148 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
limited role within traditional theories of associa-
tive learning (e.g. Hull, 1943; Rescorla and Wag-
ner, 1972; Mackintosh, 1975; Pearce and Hall,
1980; Pearce, 1987; but see Gibbon and Balsam,
1981; Gallistel, 1990; Sutton and Barto, 1990).
The prevailing view has been that animals do not
learn about the temporal properties of the stimu-
lus events in Pavlovian conditioning experiments.
Recently, however, the temporal coding hypothesis
has questioned that assumption (Matzel et al.,
1988; Barnet et al., 1991; Miller and Barnet,
1993). The present paper provides an overview of
the accumulating evidence that animals do indeed
acquire (and use) temporal information in a wide
variety of Pavlovian paradigms. We discuss the
theoretical implications of temporal coding, while
emphasizing the challenges this evidence poses for
the prevailing view of associative learning.
The prevailing framework views an association
simply as a mental link between the representa-
tions of the associated events. Consider a typical
Pavlovian task: an associatively neutral condi-
tioned stimulus (CS), such as a tone, is forward-
paired in time with (i.e. occurs immediately prior
to) an unconditioned stimulus (US), such as food,
footshock, or some other event of inherent biolog-
ical significance. Following a number of these
CS – US pairings, the presentation of the CS is
said to activate in memory a representation of
that CS, which in turn activates a representation
of the US. The CS comes to elicit a conditioned
response (e.g. salivation in anticipation of food)
through a mediating association with the US.
Traditionally, the magnitude of the conditioned
response has been interpreted as direct evidence of
the strength of the CS – US association. Although
temporal factors, such as the proximity of the CS
and US during training, are presumed to con-
tribute to the strength of the association, the
assumption has been that the temporal informa-
tion itself does not become a part of that associa-
tion. Thus, temporal factors serve only a
facilitative role in the formation of associations.
The closer the two events are in time during
training, the more robust the resulting association
is presumed to be. However, an organism acquires
no representational knowledge about the tempo-
ral relationship of the paired stimulus events.
The temporal coding hypothesis represents a
radical departure from the traditional view about
the role of temporal information in associative
learning. According to the temporal coding view,
an association consists of more than a mental link
between the representations of two paired events.
Rather, the temporal relationship between the
events that prevailed during training is encoded as
part of the association. Thus, the temporal condi-
tions (e.g. the CS–US interstimulus interval) are
not merely catalysts in the formation of associa-
tions, but are also a part of the content of learn-
ing. In Pavlovian conditioning, an animal learns
not only that a US will occur, but also when the
US will occur. According to the temporal coding
hypothesis, good contiguity (i.e. temporal proxim-
ity) is sufficient for the formation of an associa-
tion, where good contiguity is defined as similar
or identical onsets of the two events. Whether an
association will be expressed as observable behav-
ior, however, depends (in part) on the encoded
temporal knowledge. The temporal information
that is acquired during training is presumed to
play a critical role in determining the nature,
magnitude, and timing of the observed condi-
tioned response. Therefore, unlike most theories
of associative learning (Rescorla and Wagner,
1972; Mackintosh, 1975; Pearce and Hall, 1980)
which have tended to treat performance as direct
evidence of learning, the temporal coding hypoth-
esis maintains a clear distinction between learning
and the behavioral expression of that learning.
That is, certain temporal relationships mitigate
against the behavioral expression of an acquired
CS–US association. As we shall see, the distinc-
tion between learning and performance is justified
by data obtained with recently developed tech-
niques that have been effective in revealing associ-
ations that would otherwise remain behaviorally
silent.
2. The mechanism of learning: contiguity versus
information
The assumption of the temporal coding hypoth-
esis that temporal contiguity is sufficient for asso-
ciative learning marks a return to the early views
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
of Pavlov (1927) and the British empiricists before
him (e.g. Locke, 1974), who believed that the
occurrence of two events in close temporal prox-
imity was the critical determinant of learning.
Since Pavlov’s time, however, the principle of
contiguity has encountered numerous empirical
challenges and, until recently, was all but aban-
doned. Perhaps the greatest challenge was the
relative ineffectiveness of simultaneous (the CS
and US have identical onset and termination
times) and backward (the CS onsetting at the
termination of the US) conditioning procedures in
producing observable conditioned responding.
Pavlov (1927) himself discovered that conditioned
responding is typically stronger after forward pair-
ings (in which the CS precedes the US) than after
training in which the CS and US are paired in a
simultaneous (i.e. CS:US) or backwards (i.e.
US “CS) manner. On the basis of contiguity
alone, one would expect simultaneous condition-
ing to produce the strongest conditioned respond-
ing because simultaneous conditioning is an
instance of perfect contiguity, whereas forward
and backward conditioning are instances of im-
perfect contiguity. Similarly, forward and back-
ward serial pairings (with equivalent durations for
the CS and US) should yield equivalent learning
because the two temporal orderings provide
equivalent contiguity. Jointly, the response deficits
observed with backward and simultaneous condi-
tioning appeared to contradict the view that bet-
ter temporal contiguity resulted in stronger
associative learning. Because these deficits were
interpreted as evidence of weak learning, grave
doubt was cast upon the view that simple contigu-
ity was the mechanism responsible for associative
149
association between their representations. Instead,
learning is presumed to occur only when one
event (nonredundantly) predicts the occurrence of
another. Thus, a CS must provide anticipatory
information about the US for associative learning
to occur. A natural account of the superiority of
forward conditioning over backward and simulta-
neous conditioning falls out of information the-
ory. Stronger responding is observed in forward
conditioning because only in that arrangement
does the CS predict the occurrence of the US.
Conversely, simultaneous and backward paired
CSs have little or no predictive value with respect
to the US, and therefore do not become associ-
ated with the US. By (implicitly) equating ob-
served responding with associative strength, the
informational hypothesis attributes the relative
ineffectiveness of simultaneous and backward
preparations to the absence of learning.
The informational hypothesis garnered further
support from a classic study by Rescorla (1968).
In a study of conditioned suppression in rats,
Rescorla showed that an equivalent number of
tone“ shock pairings might or might not result in
the tone eliciting a strong conditioned response,
depending on the number of additional shocks
delivered in the absence of the tone during the
conditioning session. This finding appeared trou-
blesome for the contiguity view. Because the de-
gree of CS–US contiguity remained unchanged
by the presentation of unsignaled USs, condi-
tioned responding to the CS should not have been
affected by the presentation of additional USs.
Instead, conditioned responding was directly infl-
uenced by the contingency between the CS and
US. Rescorla defined contingency as the probabil-
learning (for a review, see Moore and Gorme- ity of the US in the presence of the CS (p[USCS])
zano, 1977). As a result, various alternative mech- minus the probability of the US in the absence of
anisms were proposed to explain the superiority
of forward conditioning relative to simultaneous
and backward conditioning.
The informational hypothesis (Egger and Miller,
1963; Kamin, 1969; Rescorla, 1972; Rescorla and
Wagner, 1972; Cantor, 1981) emerged as perhaps
the most-widely accepted alternative to the princi-
ple of contiguity. According to the informational
hypothesis, the mere contiguous occurrence of
two events is not sufficient for the formation of an
the CS (p[USno CS]), and reasonably argued that
it served as a direct measure of the predictiveness
of the CS. (Notably, this definition of contingency
has been adopted by several theories of human
causal judgment as a normative index of the
statistical correlation between two events e.g. Al-
lan, 1993; Cheng, 1997). As is discussed below,
the notion of the informational hypothesis that a
nonredundant predictive relationship is critical for
engaging the learning mechanism was also able to
150 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
account for the so-called ‘cue-competition’ phe-
nomena, such as o6ershadowing and blocking,
wherein stimuli that are trained together, accord-
ing to the informational view, compete for asso-
ciative linkage to a common US. In contrast,
simple contiguity theory cannot explain the re-
sponse deficits that result from cue competition
because the competing stimuli are contiguous with
the US and consequently should become associ-
ated with it. Cue competition phenomena served
as the basis for many of the current models of
Pavlovian conditioning (Rescorla and Wagner,
1972; Mackintosh, 1975; Pearce and Hall, 1980),
all of which hold (nonredundant) prediction to be
a requirement for learning to occur.
The informational hypothesis, however, en-
counters problems when applied to backward and
simultaneous conditioning. The theory maintains
that only stimuli that have predictive value should
acquire excitatory status. However, several results
in the human and animal learning literatures
provide evidence that a forward temporal rela-
tionship is not necessary for the establishment of
an association between stimuli. For instance, hu-
man learning theorists are less concerned with the
temporal relationship between stimuli because
strong associations are seemingly formed between
stimuli presented simultaneously in preparations
such as the paired-associates task in which a list
of word pairs is presented to subjects (e.g. Gib-
son, 1940). Within the animal literature, Rescorla
(1980) controlled for certain problems that con-
founded earlier studies of simultaneous condition-
ing (i.e. distraction from one stimulus by another
of higher salience), and found that the association
between simultaneously presented neutral stimuli
is stronger than the association formed between
an antecedent cue and an immediately following
stimulus. Consistent with this, Burkhardt and
Ayres (1978), using a conditioned suppression
procedure with rats, reported that, at least early in
training (i.e. after few training trials), a CS that is
paired simultaneously with a shock US will sup-
port reliable excitatory responding (see also Heth,
1976; Heth and Rescorla, 1973). Moreover, evi-
dence of robust backward associations has been
reported both in conditioned suppression prepara-
tions with rats (Ayres et al., 1987) and pigeon
autoshaping (Hearst, 1989). In Hearst’s study, a
stimulus that had only followed brief periods of
available food proved much easier to convert into
an effective signal for food than did a stimulus
that had been uncorrelated with food. Therefore,
although responding to a forward conditioned CS
is generally stronger than to a backward or simul-
taneous conditioned CS, the foregoing demonstra-
tions of successful backward and simultaneous
conditioning are problematic for the view that
predictive value is essential for learning to occur.
The informational hypothesis has appealed to
researchers in large part because it conforms
nicely to an evolutionary framework that empha-
sizes the functional nature of learning. Predictive
learning is seemingly functional to the extent that
it enables an organism to prepare for (and per-
haps modify) the occurrence of biologically sig-
nificant events. As argued by Mackintosh (1983),
conditioning, from a functional standpoint,
should provide the subject with information about
the impending reinforcer. However, one problem
with an evolutionary approach is that ultimate
functions of behavior are sometimes confused
with proximate mechanisms. Whereas a likely ul-
timate function of learning is to allow organisms
to anticipate significant events, the proximate
mechanism responsible for the ability to predict
significant events might well be a simpler mecha-
nism that is sensitive to temporal contiguity rather
than predictive value. But, if temporal contiguity
is to be considered a viable mechanism of associa-
tive learning, we need an explanation of why
behavioral control resulting from simultaneous
and backward pairings is generally weaker than
that resulting from forward pairings, despite for-
ward associations being weaker than simultaneous
and equal to backward associations in terms of
contiguity.
3. The temporal coding hypothesis
Most Pavlovian tasks are designed to measure
responses that are anticipatory in nature (e.g.
salivating in anticipation of food, blinking the
eyes in anticipation of an air puff, freezing in
anticipation of footshock). Thus, one alternative
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
to the informational account is the possibility that
simultaneous and backward pairings result in well
learned associations, but that the CS does not
generally evoke a conditioned response with con-
ventional measures of Pavlovian association be-
cause it does not bear a forward (predictive)
relationship to the US. Conventional measures of
Pavlovian associative strength may be appropriate
for the expression of forward associations, but
they would likely be inadequate for the expression
of backward or simultaneous associations. Thus,
the weak conditioned response observed in those
situations might not reflect a failure to engage the
learning system during training, but rather an
inability to engage the appropriate response sys-
tem.
This is essentially the position taken by the
temporal coding hypothesis (Matzel et al., 1988;
Barnet et al., 1991; Miller and Barnet, 1993),
which can be summarized as follows; (1) Contigu-
ity alone is necessary and sufficient for the forma-
tion of an association. (2) The temporal
relationship between the associated events is auto-
matically encoded as part of the association (i.e.
subjects form temporal maps that link events in
memory). (3) This temporal information plays a
critical role in the nature, magnitude, and timing
of the conditioned response elicited when one of
the associates is subsequently presented. Finally,
(4) animals can superimpose temporal maps when
elements common to these maps are presented
together, even when the elements were trained
separately. That is, temporal information from
different training situations can be integrated.
According to this view, simultaneous and back-
ward associations, as well as forward associations,
can be learned as long as good CS – US contiguity
exists. However, the expression of that learning
requires a predictive relationship between the CS
and the US, at least when the typical anticipatory
response systems are measured. Thus, information
about an upcoming US supports anticipatory re-
sponding to the CS, which ordinarily prepares the
subject for the impending US. However, a predic-
tive relationship is not essential for associative
acquisition. Accordingly, the commonly observed
response deficit following simultaneous or back-
ward CS–US pairings, relative to forward CS –
151
US training, is attributed to different temporal
information being encoded during simultaneous
or backward pairings, rather than to a failure in
associative acquisition per se.
4. Assessing simultaneous and backward
associations
If simultaneous and backward associations are
latent, the question arises about how their exis-
tence can be assessed. It is unclear whether a
direct measure is possible because it is not certain
what response systems are specifically appropriate
to the expression of simultaneous and backward
associations. However, Farley and Alkon (1987)
obtained some intriguing data with the mollusk
Hermissenda. They paired a light CS which nor-
mally elicits a positive phototactic response in this
species with high-speed rotation of the subject, an
aversive US that normally suppresses phototaxis.
Depolarization of the Hermissenda’s photorecep-
tor to the light served as the index of associative
strength. They found stronger conditioning (i.e.
greater suppression [decreased photoreceptor de-
polarization] to the light) with simultaneous
CS:US pairings than with forward CS“ US pair-
ings. These studies are interesting because, rather
than monitoring a response system that depends
on the anticipation of the US for its expression,
Farley and Alkon indexed associative strength
more directly, that is, at the neural level prior to
the translation of that information into higher-or-
der response systems. Similar results have been
reported in other studies in which associative
learning was also monitored at the neural level
(Kandel and Schwartz, 1982).
In more conventional Pavlovian preparations,
the existence of simultaneous and backward asso-
ciations can be assessed indirectly, through the
use of a second-order conditioning procedure. In a
second-order conditioning procedure, a first-order
stimulus (CS1) is forward-paired with the US in
Phase 1 (CS1“ US), and subsequently a second-
order stimulus is forward-paired with CS1 (in the
absence of the US) during Phase 2 (CS2“ CS1).
During testing, a strong conditioned response is
observed to CS2 (relative to control groups lack-
152 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
ing either the Phase 1 or Phase 2 experience), even
though CS2 was never itself directly paired with
the US. For the purpose of assessing the existence
of simultaneous or backward associations, sec-
ond-order conditioning is useful because it allows
for testing a simultaneous or backward CS1 – US
association through observation of responding to
CS2, which has a predictive relationship with
CS1, thereby allowing the expression of the CS1 –
US association. For example, in a study of condi-
tioned lick-suppression in water-deprived rats,
Barnet et al. (1991) trained the first-order cue
(CS1, an auditory cue) simultaneously with the
US (CS1:US, the US being a mild footshock), and
subsequently paired a second-order cue (CS2, a
different [counterbalanced] auditory cue) in a for-
ward (predictive) manner with CS1 (CS2 “ CS1).
Even though CS1 elicited little responding (i.e.
low conditioned suppression of ongoing drink-
ing), which was consistent with the expected
simultaneous conditioning deficit, a strong condi-
tioned response was observed to CS2. That is, a
strong simultaneous (CS1 – US) association was
revealed by creating a predictive relationship be-
tween CS2 and CS1, and hence indirectly between
CS2 and the US. Presumably, the CS2-US tempo-
ral relationship was the consequence of integra-
tion of the CS1–US and CS2 – CS1 temporal
relationships because CS2 was never directly
paired with the US. (Note that this view can
account for the previously described data of Res-
corla (1980) without recourse to the notion of
distraction. That is, Rescorla may have obtained
strong responding to his test stimulus, not because
there was no simultaneous US, but because his
test stimulus had an anticipatory relationship to
the first-order simultaneous CS.)
Another procedure that is useful for detecting
simultaneous and backwards associations is sen-
sory preconditioning (Brogden, 1939). This proce-
dure is similar to second-order conditioning,
except that the order of the training phases is
reversed (i.e. CS2–CS1 pairings precede the first-
order conditioning CS1 – US trials). The phe-
nomenon of sensory preconditioning is
theoretically intriguing because it demonstrates
that organisms can associate and time events that
are not biologically significant at the time of
training. For the purpose of assessing associations
that are latent because of their putative temporal
content, sensory preconditioning provides another
means of creating a predictive association that
provides a measure of a simultaneous or back-
ward association. For example, Matzel et al.
(1988) initially exposed rats to forward CS2“
CS1 pairings followed by either forward, simulta-
neous, or backward pairings of CS1 with the US.
Once again, the expected simultaneous and back-
ward response deficits were observed to CS1.
However, CS2, which had been established as a
predictor of CS1 (and hence presumably a predic-
tor of the US), evoked a strong conditioned re-
sponse regardless of the manner in which CS1 had
been paired with the US.
Jointly, the studies of Barnet et al. (1991) and
Matzel et al. (1988) provide clear evidence that
animals acquire strong simultaneous and back-
ward associations in conventional Pavlovian
preparations. However, that information was ex-
pressed when and only when the acquired infor-
mation was of functional, predictive value
appropriate for the anticipatory response system
that was monitored. Thus, these findings are con-
sistent with the view of the temporal coding hy-
pothesis that simple contiguity is sufficient for
associative acquisition, but that the expression of
learning ordinarily requires a predictive relation-
ship when assessed by an anticipatory measure. In
these studies, higher-order stimuli were estab-
lished as predictors of first-order stimuli that had
backward or simultaneous associations with the
US. The implication is that the temporal relation-
ship between a paired CS and US was encoded
and integrated with the memory for the higher-or-
der stimulus (i.e. CS2). In this manner, the tempo-
ral coding hypothesis not only explains the
behavioral silence of first-order backward and
simultaneous associations, but also offers a plau-
sible account of second-order conditioning and
sensory preconditioning.
Furthermore, the strong simultaneous and
backward associations revealed in those studies
are consistent with previous reports of simulta-
neous and backward associations (e.g. Hearst,
1989). Collectively, these findings attest to the
sufficiency of contiguity as the basic requirement
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162 153

of learning, and contradict the view that predic-
tion is necessary to support an association be-
tween stimulus events. Moreover, they are
incompatible with the conclusion that the rela-
tively weak responding generally observed after
simultaneous and backward conditioning reflects
a learning deficit. Contrary to the informational
accounts and ‘prevailing wisdom’, the magnitude
of the conditioned response in those cases is not
necessarily a reliable indicator of underlying asso-
ciative strength. Thus, the learning-performance
distinction proposed by the temporal coding hy-
pothesis appears to be justified.
forward (CS1“ US) first-order pairings. The
magnitude of responding to the higher-order con-
ditioned stimulus was determined by a memory
representation, constructed from the two phases
of training, that provided information about the
expected temporal location of the US.
Cole et al. (1995) reported another intriguing
demonstration of temporal integration in trace
conditioning. In trace conditioning, a temporal
gap is inserted between the offset of the CS and
the onset of the US. This typically results in
weaker conditioned responding than does a stan-
dard forward control (with no gap; i.e. delay
conditioning). Cole et al. gave first-order CS1–US

5. Temporal integration

The results of the higher-order conditioning

studies just described imply that animals integrate
temporal relationships from different associations
that share a common stimulus. A rather com-
pelling demonstration of temporal integration,
congruent with the temporal coding hypothesis,
was reported by Barnet et al. (1997). With both
second-order conditioning (Experiment 1) and
sensory preconditioning (Experiment 2) proce-
dures, they exposed rats to either backward
(US “ CS1) or forward (CS1“ US) first-order
training. CS2 was always conditioned in a for-
ward manner with CS1 (CS2“CS1). Not surpris-
ingly, responding to CS1 was superior in the
forward case than the backward case. However,
the magnitude of conditioned responding to CS2
was actually greater with the backward first-order
pairings than with the forward first-order pair-
ings. This superiority of backward pairings is
entirely consistent with the idea that temporal
relationships from different phases of training are
encoded as memory representations and inte-
grated into a single representation that determines Fig. 1. Presumed event representations and temporal relation-
ships of a Forward (A) or Backward (B) first-order association
the nature and strength of the conditioned re- (Phase 1) integrated (superimposed) with those of a forward
sponse. Fig. 1 illustrates the presumed integration second-order (CS2 “CS1) association (Phase 2). Arrow length
of first-order and second-order associations based represents the temporal expectancy for the onset of the US
on superpositioning of their common element signaled by the onset of CS2. Font size under Test CS2
(CS1). As denoted by the length of the arrows, the indicates the magnitude of the predicted and observed condi-
tioned response. Barnet et al. (1997) assessed conditioning by
expected temporal location of the US following the ability of CS2 to suppress ongoing drinking in water-de-
the onset of CS2 is more proximate with back- prived rats. Mean times to reinitiate drinking are presented in
ward (US“ CS1) first-order pairings than with parentheses.
154 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
Fig. 2. Presumed event representations and temporal relation-
ships of a delay (A) or trace (B) first-order association (Phase
1) integrated (superimposed) with those of a backward second-
order (CS1 “ CS2) association (Phase 2). Arrow length repre-
sents the temporal expectancy for the onset of the US signaled
by the onset of CS2 in the Trace condition; there is no arrow
for the Delay condition because CS2 and the US have simulta-
neous onsets in the integrated representation. Font size under
Test CS2 indicates the magnitude of the predicted and ob-
served conditioned response. Cole et al. (1995) assessed condi-
tioning by the ability of CS2 to suppress ongoing drinking in
water-deprived rats. Mean times to reinitiate drinking are
presented in parentheses.
pairings with either a 5-s gap or no gap, followed
in Phase 2 by backward second-order condition-
ing (CS1“ CS2). They observed, relative to delay
conditioning of CS1, the expected trace deficit in
conditioned responding to CS1. Moreover, they
confirmed the counterintuitive prediction of the
temporal coding hypothesis that greater second-
order conditioning should occur following trace
first-order pairings than following delay first-or-
der pairings. Fig. 2 illustrates this prediction by
superimposing the representations of the common
element from the two phases of training (CS1).
The onset of CS2 signals a predictive relationship
to the US only in the trace condition, not in the
delay condition. Thus, the greater second-order
responding observed in the trace condition can be
accounted for by assuming that responding to
CS2 depended upon the integration of the memo-
ries (i.e. temporal maps) for the two phases of
training and the resultant expected temporal loca-
tion of the US with respect to CS2.
6. Temporal coding in cue competition
In addition to second-order conditioning and
sensory preconditioning, there is emerging evi-
dence that temporal attributes are also encoded in
other Pavlovian preparations. Particularly, a
number of recent studies have examined the role
of temporal encoding in the cue competition
paradigms. ‘Cue competition’ is said to occur
when two (or more) conditioned stimuli are
trained in compound with a common US and are
seen to compete with each other for behavioral
control based on the occurrence of the US. Spe-
cifically, an impaired conditioned response is seen
to a CS that is trained in the presence of another
stimulus that is more salient (i.e. overshadowing)
or a better predictor of the US (i.e. blocking).
(Notably, the effect of degrading the CS-US con-
tingency by adding unsignaled US’s can be viewed
as an instance of cue competition, wherein contex-
tual cues provided by the experimental chamber
acquire predictive value and thus come to block
responding to the CS.) As previously stated, the
cue competition phenomena have played an im-
portant role in the development of the informa-
tion-based theories of associative learning, such as
the influential Rescorla and Wagner (1972) model
and many of its modern competitors (Mackin-
tosh, 1975; Pearce and Hall, 1980). According to
all of these theories, the stimulus that has greater
predictive value will acquire a larger portion of
the available associative strength at the expense of
the less predictive (or salient) stimulus. Thus,
these theories explain the response deficits ob-
served following cue competition treatments as
failures of learning.
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
In the typical blocking experiment, for example,
a stimulus (A) is initially paired with the US
(A “US). In a second phase of training, Stimulus
A is presented together with another stimulus (X)
and paired with the US (AX “ US). During sub-
sequent testing, responding to X alone is found to
be impaired relative to responding to X in sub-
jects that received the AX“ US trials without the
prior A “US trials. Information theories at-
tribute this effect to the previously accrued predic-
tive value of Stimulus A, which is said to have
‘blocked’ acquisition of an X – US association. In
a series of experiments, Barnet et al. (1993) (see
also Schreurs and Westbrook, 1982) examined the
role of temporal coding in blocking. During Phase
1, the blocking Stimulus A was either simulta-
neously or forward paired with the US. In Phase
2, Stimulus A was presented in simultaneous com-
pound with the target Stimulus X that was paired
in a simultaneous or forward manner with the
US. Robust blocking of a forward X “ US associ-
ation was evident if the blocking Stimulus A had
been pretrained in a forward manner. Similarly
robust blocking of a simultaneous X-US associa-
tion was evident if A had been trained simulta-
neously in Phase 1. However, a forward A“ US
association produced little blocking of a simulta-
neous X–US association, and a simultaneous A –
US association produced little blocking of a
forward X“ US association. (Second-order con-
ditioning was used to assess all associations be-
cause first-order simultaneous associations are
usually behaviorally silent.) These results suggest
that information concerning the temporal location
of the US provided by the pretrained stimulus
determined the amount of blocking observed.
Blocking was greatest when the blocking and
blocked CSs shared the same temporal relation-
ship with the US. Although blocking clearly does
occur with nonsimultaneous CSs (Kehoe et al.,
1981), Barnet et al.’s data suggest that blocking
will be greater with simultaneous CSs than non-
simultaneous CSs. Such a dependence on CS – US
temporal relationships provides strong evidence
that such temporal information is encoded as part
of CS–US associations.
Temporal encoding has also been shown to
play an important role in the phenomenon of
155
overshadowing. Overshadowing refers to the
deficit in conditioned responding observed to a
CS that was trained in the presence of a more
salient CS (i.e. of higher intensity). Blaisdell et al.
(1998a), in a study of conditioned lick-suppression
with rats, used a preparation in which a bright
flashing light would overshadow a soft tone. In a
series of experiments, they systematically varied
the overshadowed CS–US temporal relationship
and the overshadowing CS–US temporal rela-
tionship. They found support for the prediction of
the temporal coding hypothesis that overshadow-
ing should be maximal when the overshadowing
and overshadowed CSs share the same temporal
relationship with the US. That is, overshadowing
of a CS with a forward, simultaneous, or back-
ward relationship with the US was greatest when
the overshadowing CS also had a forward, simul-
taneous, or backward relationship with the US,
respectively. (Again, all assessment was through
examination of a second-order CS which revealed
otherwise silent simultaneous and backward asso-
ciations.) In a more recent series of experiments,
Blaisdell et al. (1998b) demonstrated that the
overshadowing deficit could be alleviated by
changing the temporal relationship between the
overshadowing stimulus and the US after over-
shadowing treatment. That is, overshadowing of
X was attenuated if the temporal relationship
between the overshadowing CS (A) and US was
altered following AX“ US training, such that the
A–US temporal relationship was no longer the
same as the X–US temporal relationship.
To the extent that temporal information is au-
tomatically encoded as part of any association, as
is asserted by the temporal coding hypothesis,
conditioned responding to a stimulus with a par-
ticular temporal relationship with a US should be
better blocked or overshadowed by a stimulus
that has the same temporal relationship with the
US than by a stimulus that has a different tempo-
ral relationship with the US. The studies reviewed
here varied the temporal relationships between the
competing events and the US in cue competition
paradigms and found cue competition to be sensi-
tive to the similarity of these temporal relation-
ships. These observations cannot be explained in
terms of the CS–US intervals merely influencing
156 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
the associative strengths of the competing cues
because in some situations longer intervals be-
tween CS onset and US onset produced more
competition than did shorter intervals. Hence,
these findings further document the encoding of
temporal relationships as part of the content of
simple associations.
Moreover, these studies (e.g. Barnet et al., 1993;
Blaisdell et al., 1998a) demonstrate that cue com-
petition can occur between cues that are paired in
a non-predictive fashion as effectively as stimuli
that are paired with a US in an anticipatory
(forward) manner. Consequently, these findings
also challenge the central premise of the informa-
tional hypothesis that a cue must have predictive
value in order for it to enter into an association
with a US. Other research has confirmed that
blocked or overshadowed stimuli enter into asso-
ciations, but such associations are ordinarily la-
tent unless special steps are taken to reveal them
[e.g. recovery from overshadowing through re-
minder treatments (Kasprow et al., 1982), post-
training extinction of the overshadowing stimulus
(e.g. Kaufman and Bolles, 1982; Matzel et al.,
1985), and spontaneous recovery (Kraemer et al.,
1988), and recovery from blocking through post-
training extinction of the blocking stimulus (Blais-
dell et al., 1998c)]. Therefore, associative
acquisition does not seem to require a nonredun-
dant predictive relationship between the events to
occur.
Instead, the data are consistent with contiguity
as the guiding principle for the acquisition of
associations, but with an anticipatory relationship
being required as a rule for the expression of
those associations when anticipatory measures are
used. Associations (which we assert always in-
clude temporal information) will be formed as
long as there is sufficient contiguity between the
events to be associated, regardless of whether the
stimulus in question precedes the onset of the US.
However, whether the association will be ex-
pressed in the animal’s behavior appears to de-
pend largely on the saliency, prior conditioning
history, and temporal relationship with the US of
other cues that were present during training with
the target CS (as well as the test stimulus having
a predictive relationship to the US in most Pavlo-
vian situations). This rule for the expression of
associations with respect to cue competition is
basic to the comparator hypothesis (Miller and
Schachtman, 1985; Miller and Matzel, 1988),
which is a response rule that complements the
temporal coding hypothesis. The temporal coding
hypothesis provides both a simple rule for acquisi-
tion (i.e. contiguity) and is one of the several rules
that jointly apply to associative expression (i.e. an
anticipatory relationship to the US). Thus, the
temporal coding hypothesis is able to explain why
responding to a second-order CS is effective in
assessing simultaneous and backward first-order
associations, whereas responding to the first-order
CS is not, as well as why CSs with different
temporal relationships to a common US compete
less than do CSs with a common temporal rela-
tionship to the US. However, the comparator
hypothesis (or some other rule for the expression
of associations) is required to explain cue compe-
tition [including Rescorla (1968) degraded contin-
gency effect] in the first place. Therefore, the
temporal coding hypothesis and the comparator
hypothesis complement each other in providing a
complete explanation of Pavlovian conditioning.
7. Temporal coding in the Hall–Pearce
CS-preexposure effect
A well-known finding in the Pavlovian litera-
ture is the CS-preexposure effect, also known as
‘latent inhibition’ (Lubow and Moore, 1959). If a
CS is presented alone for a number of trials prior
to the start of conditioning (i.e. pairing of the CS
with a US), the emergence of conditioned re-
sponding is retarded (i.e. requires more CS–US
pairings) relative to a control group lacking the
CS-preexposure trials. Hall and Pearce (1979) re-
ported a phenomenon similar to the CS-preexpo-
sure effect. In their study, the preexposure phase
consisted of pairing the CS with a low intensity
version of the US in Phase 1 (CS “ USweak) fol-
lowed by pairings with a higher-intensity version
of the US in Phase 2 (CS“ USstrong). This resulted
in weaker responding to the CS than was ob-
served in subjects lacking the Phase 1 experience
with the target CS. In a recent study, Savastano et
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
al. (1998) examined the role of temporal encoding
in this preexposure effect. They either varied or
kept constant the temporal gap between CS termi-
nation and US onset across the two training
phases. They found that varying the gap, regard-
less of whether it was lengthened or shortened
between Phase 1 and Phase 2, resulted in less of
an impairment of conditioned responding than
did equivalent gaps in the two training phases,
thereby suggesting that the temporal relationship
learned in Phase 1 had been encoded. Thus, these
observations further support the view that the
temporal relationship between a CS and a US is
automatically encoded as part of the content of a
Pavlovian association.
8. Temporal coding in conditioned inhibition
Thus far, our discussion has been limited to the
role of temporal information in excitatory condi-
tioning, that is, how subjects use temporal infor-
mation in anticipating when a US is going to
occur. However, recent evidence suggests that
temporal encoding also plays a role in inhibitory
conditioning. A conditioned inhibitor is a stimu-
lus that signals the omission of a US that in the
absence of the signal would be expected. In a
typical Pavlovian inhibition procedure, one stimu-
lus (the training excitor) is paired with the US
when it is presented alone (A“US), but not when
it is presented in compound with the intended
inhibitor (AX-). Typically, A“US and AX- trials
are interspersed within a session. The inhibitory
power of the putative inhibitor (X) is then com-
monly assessed through a summation test, which
entails presenting X in the presence of an indepen-
dently trained excitatory stimulus (B, which is
called a transfer excitor). Conditioned inhibition
is evidenced by a reduced conditioned response to
the BX compound relative to the transfer excitor
(B) alone. The question here is whether an in-
hibitory stimulus provides information about the
temporal location of the omitted US in the same
way that an excitatory CS provides temporal in-
formation about the presentation of the US. In a
recent study of conditioned-lick suppression with
rats, Barnet and Miller (1996) gave subjects
157
Pavlovian conditioned inhibition training (A-US/
AX-) in which (1) the intended inhibitor (X) and
the training excitor (A) were paired either in a
simultaneous (AX-) or forward manner (X“ A-),
and (2) the training excitor was either simulta-
neously (A:US) or forward-paired (A“US) with
the US. The transfer excitor (B) was always for-
ward-paired with the US (B“ US). Inhibitory
conditioning was found to be maximal when the
time at which the US was expected to be omitted
(the temporal information activated by the in-
hibitor based both on its relationship to the train-
ing excitor and the training excitor’s relationship
to the US) was the same as the time at which the
US was expected to be presented (the information
activated by the transfer excitor based on its
temporal relationship to the US). Specifically,
conditioned inhibition was greatest in the condi-
tions in which a simultaneous inhibitor was
trained with a forward-paired excitor or a for-
ward-paired inhibitor was trained with a simulta-
neously-paired excitor. These finding are
consistent with the idea that a conditioned in-
hibitor provides information about the temporal
location of an omitted US (see also Denniston et
al. 1998a; Denniston et al., 1998b; for additional
demonstrations of temporal coding in inhibitory
conditioning).
9. Time as associative content
Our review of the role of time in Pavlovian
conditioning has revealed that, across a wide ar-
ray of Pavlovian paradigms, the temporal rela-
tionships between associated stimulus events are
encoded by the animal as an integral part of the
interstimulus association. This view differs from
the traditional assumption that associations can
vary only along the dimension of strength. The
solution offered by the temporal coding hypothe-
sis is that associations vary along at least two
dimensions—associative strength and the tempo-
ral relationship between the associated stimulus
events. In other words, traditional associative
strength and temporal relationships can be viewed
as two dimensions of the bond between event
representations. In this sense, the temporal coding
158 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
hypothesis differs from simple contiguity theory
by asserting that, although contiguity is sufficient
for the acquisition of an association, the behav-
ioral expression of that association depends on
the temporal relationship of the associates. The
distinction between ‘what is learned’ and ‘the
behavior observed’ appears to be among the sim-
plest modifications of contiguity theory that can
permit it to account both for the behavioral si-
lence of simultaneous and backward associations,
and for the observation that subjects learn tempo-
ral relationships in a wide array of Pavlovian
situations.
Other recent theoretical developments also at-
test to the importance of temporal coding in
Pavlovian conditioning. A more extreme position
than that of the temporal coding hypothesis is
adopted by Gallistel (1990). His model abandons
the traditional notion of associative strength alto-
gether. Rather than viewing temporal relation-
ships as one of several attributes of an
association, the model assumes that Pavlovian
associations exclusively encode temporal relation-
ships. In Gallistel’s view, organisms simply ac-
quire representations of the temporal intervals
between events, and these temporal relationships
serve as the basis of behavior. However, it may be
premature to relinquish the notion of associative
strength. Consider the everyday example of our
association between a table and a chair. The
temporal relationship between them is so varied
that there is effectively no temporal relationship,
yet a strong associative linkage surely exists.
Moreover, reducing all learning to the temporal
dimension neglects other dimensions that are
seemingly encoded as part of an association. For
example, spatial information would be acquired
from the strong spatial relationship that a chair
ordinarily has to a table. We prefer to think of an
association as being the sum total of all of the
relationships that link two events, with the tempo-
ral relationship being of considerable import but
not the sole basis of the association.
Several real-time models of conditioning in
which the temporal relationship between events is
in some way encoded have been formulated re-
cently (e.g. Wagner, 1981; Sutton and Barto,
1990; Grossberg, 1991). None of these models,
however, have been applied to the range of phe-
nomena described here. Like the temporal coding
hypothesis, some real-time models (e.g. Sutton
and Barto, 1990) correctly predict that cue com-
petition will be maximal if the competing CSs
share the same temporal relationship to the US.
However, because most of these models were
derived directly from information theory and have
adopted a Rescorla–Wagner learning rule, they
are hindered by the constraint that a predictive
relationship is necessary for associative acquisi-
tion. Thus, these models would not expect the
strong simultaneous and backward associations
revealed in the second-order conditioning and
sensory preconditioning studies described above.
As such, the real-time models are unable to en-
compass the central distinction within the tempo-
ral coding hypothesis between learning (through
contiguity) and expression of acquired informa-
tion (through learned forward temporal relation-
ships).
Perhaps it should not be surprising that animals
encode temporal relationships in Pavlovian tasks.
A large literature indicates that both human and
nonhuman subjects learn to time their behavior
when doing so maximizes reward or minimizes
effort on instrumental tasks (e.g. Church, 1978;
Roberts, 1981). This is evident in many situations,
for example the scalloped response patterns gener-
ated when a fixed-interval schedule of reinforce-
ment is in effect. Even in Pavlovian conditioning,
it has long been known that subjects may time
their conditioned responses in accordance with
the duration of the CS (Pavlov, 1927). For exam-
ple, in the phenomenon called inhibition of delay,
subjects with sufficient training learn to withhold
their responses until near the end of a long CS,
just before the US is due to be presented. Thus, it
has long been recognized that when reinforcement
is involved in an association, subjects can and do
learn the temporal relationship between a signal
and reinforcement.
Sensory preconditioning demonstrates that ani-
mals can learn to associate relatively neutral stim-
ulus events. But the important question for the
present framework is whether temporal relation-
ships between neutral stimulus events are auto-
matically encoded. The series of studies by Matzel
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
et al. (1988) that was discussed previously con-
tained an additional experiment that addresses
this question directly. Rats were first exposed to
either simultaneous or forward pairings of two
neutral CSs (i.e. CS2:CS1 or CS2“ CS1, respec-
tively). In Phase 2, CS1 was made biologically
relevant by presenting it simultaneously with the
US (CS1:US). Not surprisingly, responding to
CS1 was uniformly weak because of its simulta-
neous relationship to the US. However, strong
conditioned responding to CS2 was evident, but
only when CS2 had a forward (i.e. anticipatory),
rather than a simultaneous, relationship with CS1.
These findings indicate that animals had encoded
the temporal relationship between CS1 and CS2
even though neither of these cues was biologically
relevant at the time they were paired. The sugges-
tion is that encoding of temporal relationships is
an automatic process within associative learning,
and does not require that one of the associated
events be of biological significance.
10. Evolutionary adaptiveness
Earlier we considered the possible evolutionary
advantage of an information-based learning
mechanism over a simpler contiguity mechanism.
Part of the appeal of information theory lies in
the functional value of predictiveness and its abil-
ity to explain why organisms make preparatory
responses in anticipation of biologically significant
events, but not following biologically significant
events. However, an argument could also be made
that forming associations between events on the
basis of contiguity alone is adaptive. Such a posi-
tion would have to propose an evolutionary ad-
vantage of learning simultaneous or backward
associations as well as predictive associations.
Conceivably, in our evolutionary history, situa-
tions arose in which organisms encountered a
biologically significant event simultaneously with
an initially neutral (first-order) stimulus event. At
some later point, an organism might encounter a
second neutral stimulus followed immediately by
the first-order event (i.e. an anticipatory relation-
ship). Thus, the second-order stimulus may accrue
the potential to act indirectly as an anticipatory
159
signal for the impending biologically significant
event (analogous to the second-order conditioning
procedure of Barnet et al., 1991). The organism
would be well served to prepare for the biologi-
cally significant event when it later encounters the
second-order cue. However, the organism would
be able to make a preparatory response to the
second-order stimulus only if: (a) a forward asso-
ciation was formed between the second-order
stimulus and the first-order stimulus, and (b) an
association was formed between the first-order
stimulus and the biologically significant event.
The latter (b) would only occur if simultaneous
associations could be acquired. Thus, organisms
that were not able to encode nonanticipatory as
well as anticipatory temporal relationships may
have had a lower adaptive fitness relative to or-
ganisms that were able to learn both types of
temporal relationships. The latter organisms
would have learned on the basis of contiguity
alone, but responded on the basis of integrated
information from each of the associations that
jointly allow second-order CSs to convey anticipa-
tory information about biologically significant
events. Thus, a compelling argument can be made
for the functional value of learning by contiguity,
rather than by prediction, as the critical variable
that underlies the learning mechanism. However,
at this point it is premature to categorically reject
the possibility that animals’ learning by contiguity
as opposed to learning by predictive value merely
reflects evolutionary inertia. That is, there may be
insufficient cost to animals in learning simulta-
neous and backward associations that natural se-
lection would not favor a learning mechanism
sensitive to prediction over one sensitive to conti-
guity. More significantly, the fact that compelling
evolutionary arguments exist for contiguity-based
learning as well as for prediction-based learning
points out the dangers of allowing the analysis of
proximate processes to be overly influenced by
theorizing at the level of ultimate mechanisms.
11. Bidirectional associations
Finally, a clear implication of the temporal
coding hypothesis is that associations are bidirec-
160 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
tional in nature. Consider the case in which
event A is followed by event B during training
(A“ B). Because the temporal coding hypothesis
assumes that associative learning depends on
contiguity rather than prediction, and further-
more assumes that temporal relationships are
encoded, it suggests that presenting one event
should activate the representation in memory of
the other event (as well as its temporal location
relative to the signal). For this to occur, the
association between A and B must be function-
ally bidirectional (AlB). Thus, the presentation
of A alone should activate a prospective (predic-
tive) representation of B, and testing on B alone
should activate a retrospective representation of
A.
Anecdotally, it is clear that many of our ev-
eryday associations appear to be bidirectional.
When we hear the word ‘Paris’, we might come
to imagine the popular sights of the city, such
as the Eiffel tower. If we were later shown a
picture of the Eiffel tower, we would have no
problem supplying the name of the city. In a
simple, but elegant, study, Gerolin and Matute
(1998) found empirical support for the existence
of functional bidirectional associations in human
subjects. Their subjects were trained on pairs of
neutral stimulus events (colors and figures) in a
forward direction (color“ figure). At test, sub-
jects were presented with a figure, and were able
to report the associated color, thereby suggest-
ing learning of a backward association. It is un-
clear whether this result reflects the action of a
single bidirectional association or two opposing
unidirectional associations. However, the finding
was replicated even when a single training trial
was used, making less plausible any explanation
in terms of an independent figure“color associ-
ation being formed by the onset of the color
activating a representation of the figure, which
could then be forwardly associated with the still
present color (i.e. retrospective revaluation, Van
Hamme and Wasserman, 1994).
Recent findings also appear to lend strong
support to the existence of functional bidirec-
tional associations in other species. For example
Zentall et al. (1992) used a delayed conditional
discrimination task to teach pigeons that Stimu-
lus A leads to Outcome X and Stimulus B leads
to Outcome Y. Subsequently, they observed fa-
cilitated transfer in their subjects’ learning that
X leads to A and Y leads to B (i.e. the reversed
order of previous paired events) relative to
learning that X leads to B and Y leads to A
(i.e. events that were not previously paired).
This outcome suggests that backward associa-
tions were acquired at the same time that the
forward associations were learned.
12. Conclusions
We have provided an overview of the avail-
able data suggesting that temporal coding is
ubiquitous in a wide array of Pavlovian condi-
tioning paradigms. Those data support the con-
clusion that temporal contiguity between the
representation of stimulus events is sufficient for
the formation of an association. Organisms ap-
pear to use temporal relationships as a basis for
determining the nature, magnitude, and timing
of the expression of acquired information. This
distinction between learning and performance
poses a serious challenge for the traditional the-
ories of associative learning that are based on
the notion of prediction being required for
learning to occur, but it is consistent with the
basic assumptions of the temporal coding hy-
pothesis.
Acknowledgements
Preparation of this manuscript was supported
by NIMH Grants 11704-02 (H.I. Savastano)
and 33881 (R.R. Miller). Thanks are extended
to Francisco Arcediano, Aaron Blaisdell, Dan
Burger, Jim Denniston, and Martha Escobar for
their comments on earlier versions of the
manuscript. Requests for reprints should be ad-
dressed to Ralph R. Miller, Department of Psy-
chology, SUNY-Binghamton, Binghamton, NY
13902-6000, USA, E-mail: rmiller@binghamton.
edu.
 H.I. Sa6astano, R.R. Miller / Beha6ioural Processes 44 (1998) 147–162
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