Evidence for remembering when events occurred
in a rodent model of episodic memory
Wenyi Zhou and Jonathon D. Crystal1
Department of Psychology, University of Georgia, Athens, GA 30602-3013
Communicated by Charles R. Gallistel, Rutgers, The State University of New Jersey, Piscataway, NJ, April 20, 2009 (received for review January 30, 2009)
The content of episodic memory consists of representations of
unique past events. Episodic memories are grounded in a temporal
framework (i.e., we remember when an event occurred). It has
recently been argued that episodic-like memory in rats is qualita-
tively different from human episodic memory because, rather than
remembering when an earlier past event occurred, rats used the
cue of how long ago it occurred. We asked, therefore, whether rats
remember the time of day at which they encountered a distinctive
event, in addition to what occurred and where it happened. Rats
were tested in the morning and afternoon, on separate days. A
distinctive flavor (chocolate) was replenished at a daily-unique
location at only one of these times. The interval between first and
second daily opportunities to eat (study and test, respectively) was
constant. Rats adjusted their revisits to the chocolate location at
different times of day by using time of day rather than the cue of
how long ago an event occurred. Two lines of evidence suggest
that rats remembered the time at which the distinctive event
occurred. First, under conditions in which the time of test (but not
edge of the chocolate contingency to the new test time. Second,
put in conflict, rats again used study time. Our results suggest that,
at the time of memory assessment, rats remember when a recent
episode occurred, similar to human episodic memory.
retrieval of episodic memories is analogous to traveling back in
time to experience specific events from one’s personal past
(2–4). An earlier definition focused on the content of episodic
memory, that is, answering 3 questions about a specific event:
what happened, where did it take place, and when did it transpire
(5)? We refer to this type of content as what-where-when memory.
Clayton and Dickinson (6) introduced the term episodic-like mem-
ory to emphasize that behavioral studies in animals evaluate the
content of episodic memory rather than subjective experiences.
Recent studies with nonhuman animals (6–18) suggest that
animals remember specific episodes from their past (i.e., what-
where-when memories). However, controversy has emerged
about the comparability of episodic-like memory in rodents and
episodic memory in humans (17). Roberts et al. (2, 17) suggested
that memory for when an event occurred suggests an ability akin
to mentally traveling in time to locate an event within a temporal
framework; such an ability would be similar to human episodic
memory, in which people reconstruct past experiences using an
absolute temporal dimension (1, 19, 20). By contrast, a judgment
of how long ago an event occurred is quite different from human
episodic memory. Such a judgment could also be solved by
simpler alternative mechanisms (e.g., timing an interval since a
distinctive event occurred or assessing relative familiarity of
temporally distant events). Remembering the time of day at
which an event occurred is different from an assessment of how
long ago it occurred (21). An animal’s sense of time of day
depends upon an internal circadian clock (19, 22). Because
animals have an internal circadian clock that provides informa-
tion about time of day, their knowledge about time of day does
not depend on external stimuli such as light onset or other
eople remember when a past event occurred within the time
frame of hours, days, or years (1). It has been argued that
environmental cues. Thus, we use the term time of day synony-
mously with the phase of a circadian oscillator (i.e., the propor-
tion within a 24-h cycle).
The objective of this research was to determine, at the time of
memory assessment, whether rats remember when (i.e., the time
of day at which) an earlier distinctive event occurred, in addition
to what occurred and where it happened. Rats can use how-
long-ago cues under conditions in which both when and how-
long-ago cues are available (17). Therefore, we sought behav-
ioral evidence for remembering when an event occurred by
eliminating the usefulness of how long ago an event occurred as
a temporal cue. This demonstration is important because devel-
opment of a rodent model of episodic memory may improve our
understanding of human disorders of memory (23).
Rats were placed in an 8-arm radial maze twice per day. Upon
first exposure, rats obtained their first opportunity to eat regular
rat chow and a preferred food type, chocolate. We refer to the
first feeding opportunity as first helpings. After a delay, rats were
returned to the maze. However, to obtain their second oppor-
tunity to eat chow (i.e., second helpings), they needed to avoid
revisiting locations where they obtained their first helpings
earlier that same day because the old locations no longer
provided chow. To obtain their second helpings of chocolate,
they had to revisit the same location that provided chocolate
earlier in the day, but the chocolate location replenished (or
failed to replenish) according to a temporal rule. Consequently,
obtaining chocolate at second helpings required the rat to
remember when and where they found the chocolate (what)
during their first helpings, documenting the use of what-where-
when memory. We refer to the first helpings of the day as a study
phase and the second helpings as a test phase; the first phase
second phase is a test of memories of first-helpings locations
because the rats obtain additional food by visiting the locations
that were not visited in the study phase. The delay between study
and test phases (i.e., first and second helpings) is referred to as
a retention interval.
We investigated whether rats remembered the time of day at
which they had recently encountered a distinctive food type
(chocolate) using a group of rats that served in 4 experiments in
sequence. Rats were trained in the morning and afternoon, on
separate days, but chocolate replenished at a daily-unique
location at only 1 of these times (counterbalanced across rats).
The rats searched for food (i.e., their first helpings of the day)
in an initial study phase. Subsequently, the rats searched again
for food in a test phase (i.e., their second helpings of the day) on
the same day; the delay between study and test phases was 2 min.
Chocolate was found in the maze at a randomly selected location
in their first helpings each day; for rats to obtain chocolate at
Author contributions: J.D.C. designed research; W.Z. performed research; W.Z. analyzed
data; and J.D.C. and W.Z. wrote the paper.
The authors declare no conflict of interest.
1To whom correspondence should be addressed. E-mail: firstname.lastname@example.org.
This article contains supporting information online at www.pnas.org/cgi/content/full/
June 9, 2009 ?
vol. 106 ?
no. 23 ?