Benjamin M. Basile

Frontiers in Psychology

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GENERAL COMMENTARY
published: 04 February 2015
doi: 10.3389/fpsyg.2015.00075
Rats remind us what actually counts in episodic memory
research
Benjamin M. Basile*
Section on the Neurobiology of Learning and Memory, Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda,
MD, USA
*Correspondence: benjamin.basile@nih.gov
Edited by:
Michael Beran, Georgia State University, USA
Reviewed by:
Jennifer Vonk, Oakland University, USA
Bonnie Perdue, Georgia State University, USA
Keywords: episodic, semantic, source, context, rat
A commentary on
Binding of episodic memories in the rat
by Crystal, J. D., and Smith, A. E.
(2014). Curr. Biol. 24, 2957–2961. doi:
10.1016/j.cub.2014.10.074
Think back to lunch yesterday. You likely
remember what you ate, where you sat,
who you were with, what you talked about,
and myriad other details combined in
a cohesive memory. Now think back to
lunch the day before yesterday. Though
many of the details are probably the same,
you likely do not have trouble discrimi-
nating between the two memories. This
example highlights that episodic memo-
ries, or memories for specific experiences,
contain many details bound together in
cohesive representations (Tulving, 1972;
Ranganath, 2010). Contrast episodic with
semantic memories, or memories for facts.
You may know where the cafeteria is and
that sandwiches are food, but those mem-
ories are unbound to specific events.
Tulving originally defined episodic
memory as encoding dated episodes
and their spatial relations (1972), or
“what,” “when,” and “where.” These cri-
teria were objective and testable. As the
study of episodic memory matured, the
goal posts for identifying it were repeat-
edly moved away from objective criteria
and toward subjective ones (reviewed in
Tulving, 2002). The modern definition
rests heavily on concepts like autonoetic,
or self-knowing, consciousness, which
gives episodic memory a phenome-
nal “flavor of pastness” (Tulving, 1984)
and a personal “warmth and intimacy”
(Tulving, 2001). Consequently, researchers
of human memory often rely on partic-
ipants’ verbal reports of whether their
memory is subjectively episodic, such as
in the classic remember/know paradigm
(e.g., Rajaram, 1993; Gardiner, 2001).
The result is that we often define episodic
memory in the way Supreme Court Justice
Potter Stewart famously defined obscenity:
“I know it when I see it” Stewart (1964).
Subjective reports limit the questions
researchers can answer. Imagine explain-
ing the subjective feel of episodic remem-
bering to a person who has likely never
had an episodic memory due to early brain
damage (Baddeley et al., 2001). Or test-
ing whether a bee remembers a flower’s
location with an intimate flavor of past-
ness. This clash between the subjective cri-
teria of episodic memory and the need
for objective measures, especially within
comparative psychology, has produced
much theory-driven running in circles
about what “counts” as episodic mem-
ory, but with little progress (e.g., Clayton
et al., 2003; Tulving, 2005; Suddendorf and
Corballis, 2007).
Fortunately, researchers of compara-
tive psychology have made substantial
empirical progress by ignoring, for now,
the subjective criteria for episodic mem-
ory and instead asking how different
species remember past events (Templer
and Hampton, 2013b). A recent report
from Crystal and Smith (2014) highlights
the strength of this approach. Episodic
memories are characteristically cohesive;
consider the opening example. To test
the degree to which rats’ memories were
similarly bound into cohesive episodes,
Crystal and Smith tested rats’ memories
for foraging episodes that shared many
individual features. In each episode, rats
encountered several pieces of food on an
eight-arm maze. If they found a piece of
chocolate themselves, another piece would
be in the same location later. But if they
learned the chocolate’s location by being
placed there by the experimenter, or if they
found rat chow, that location would be
empty later. They engaged in two forag-
ing episodes on identical mazes in two
different rooms, which could be differ-
entiated by global visual cues. Thus, the
two foraging episodes shared many over-
lapping features. To earn as much choco-
late as possible, rats had to remember not
only which food they found, where they
found it, how they learned that informa-
tion, and in which room they foraged,
but also bind those features together into
a cohesive memory that was distinguish-
able from another memory with similar
features.
The rats successfully remembered the
foraging episodes, revisiting the replen-
ishing chocolate more often than the
non-replenishing chocolate. Importantly,
they did not confuse the two similar
foraging episodes. They remembered
two episodes as accurately as they
remembered one. They remembered
episodes that shared many features as
accurately as episodes that shared few
features. They could even distinguish
the two episodes following a week’s
delay, demonstrating that their mem-
ory was long-lasting, like many human
episodic memories. The absence of con-
fusion suggests the rats did not remember
each foraging event as a collection of
isolated features, but rather as a cohesive
whole.
www.frontiersin.org February 2015 | Volume 6 | Article 75 | 1
Basile Rats remind us
This study is one of a growing num-
ber within comparative psychology, many
by Crystal and colleagues, that highlight
how empirically productive the field can
be when it focuses on testable criteria.
Clearly, there is value to knowing whether
nonhumans and humans remember past
events similarly. We want to know how
similar we are to other species, know
how cognitive processes evolved, and iden-
tify behaviorally-valid animal models for
biomedical advancement. But we cannot
test the subjective feeling of pastness in
nonhumans. We must identify similari-
ties and differences by focusing on those
characteristics of episodic memory that
are objectively testable. We know more
than ever about the degree to which
other species remember multiple fea-
tures of events (Clayton and Dickinson,
1998; Hampton et al., 2005; Babb and
Crystal, 2006), the source of information
(Crystal et al., 2013), incidental informa-
tion (Zentall et al., 2001; Zhou et al., 2012),
the temporal order of events (Fortin et al.,
2002; Templer and Hampton, 2013a), rec-
ollectively (Menzel, 1999; Fortin et al.,
2004; Basile and Hampton, 2011), explic-
itly (Sutton and Shettleworth, 2008; Basile
et al., 2015), and over long periods of time
(Crystal and Babb, 2008; Martin-Ordas
et al., 2013). This list is not exhaustive,
but it shows that the field has amassed
an impressive knowledge of how different
species remember past events, revealing
both similarities and differences.
Because we have made little progress in
the theoretical debate about what “counts”
as episodic memory, and great progress
in the empirical study of how differ-
ent species remember events, the field
might benefit from a more explicit rejec-
tion of the very debate itself. It is easy
to get caught up in the debate about
what “counts” as episodic memory, and
to see each new piece of evidence as
weighing on one side or the other. The
recent report from Crystal and Smith
should remind us that we make the most
progress when we ignore intractable the-
oretical debates and continue gathering
data.
ACKNOWLEDGMENTS
I thank Emily Kathryn Brown and Victoria
L. Templer for feedback on an early
draft of this commentary. This work was
supported by the Intramural Research
Program of the National Institute of
Mental Health.
REFERENCES
Babb, S. J., and Crystal, J. D. (2006). Episodic-like
memory in the rat. Curr. Biol. 16, 1317–1321. doi:
10.1016/j.cub.2006.05.025
Baddeley, A. D., Vargha-Khadem, F., and Mishkin, M.
(2001). Preserved recognition in a case of develop-
mental amnesia: implications for the acquisition of
semantic memory? J. Cogn. Neurosci. 13, 357–369.
doi: 10.1162/08989290151137403
Basile, B. M., and Hampton, R. R. (2011).
Monkeys recall and reproduce simple shapes
from memory. Curr. Biol. 21, 774–778. doi:
10.1016/j.cub.2011.03.044
Basile, B. M., Schroeder, G. R., Brown, E. K., Templer,
V. L., and Hampton, R. R. (2015). Evaluation of
seven hypotheses for metamemory performance in
rhesus monkeys. J. Exp. Psychol. Gen. 144, 85–102.
doi: 10.1037/xge0000031
Clayton, N. S., Bussey, T. J., and Dickinson, A.
(2003). Can animals recall the past and plan for
the future? Nat. Rev. Neurosci. 4, 685–691. doi:
10.1038/nrn1180
Clayton, N. S., and Dickinson, A. (1998). Episodic-
like memory during cache recovery by scrub jays.
Nature 395, 272–274. doi: 10.1038/26216
Crystal, J. D., Alford, W. T., Zhou, W., and Hohmann,
A. G. (2013). Source memory in the rat. Curr. Biol.
23, 387–391. doi: 10.1016/j.cub.2013.01.023
Crystal, J. D., and Babb, S. J. (2008). Spatial memory
in rats after 25 hours. Learn. Motiv. 39, 278–284.
doi: 10.1016/j.lmot.2008.03.002
Crystal, J. D., and Smith, A. E. (2014). Binding
of episodic memories in the rat. Curr. Biol. 24,
2957–2961. doi: 10.1016/j.cub.2014.10.074
Fortin, N. J., Agster, K. L., and Eichenbaum, H. B.
(2002). Critical role of the hippocampus in mem-
ory for sequences of events. Nat. Neurosci. 5,
458–462. doi: 10.1038/nn834
Fortin, N. J., Wright, S. P., and Eichenbaum, H.
(2004). Recollection-like memory retrieval in rats
is dependent on the hippocampus. Nature 431,
188–191. doi: 10.1038/nature02853
Gardiner, J. M. (2001). Episodic memory and auto-
noetic consciousness: a first-person approach.
Philos. Trans. R. Soc. B Biol. Sci. 356, 1351–1361.
doi: 10.1098/rstb.2001.0955
Hampton, R. R., Hampstead, B. M., and Murray,
E. A. (2005). Rhesus monkeys (Macaca mulatta)
demonstrate robust memory for what and
where, but not when, in an open-field test
of memory. Learn. Motiv. 36, 245–259. doi:
10.1016/j.lmot.2005.02.004
Martin-Ordas, G., Berntsen, D., and Call, J. (2013).
Memory for distant past events in chimpanzees
and orangutans. Curr. Biol. 23, 1438–1441. doi:
10.1016/j.cub.2013.06.017
Menzel, C. R. (1999). Unprompted recall and
reporting of hidden objects by a chimpanzee
(Pan troglodytes) after extended delays. J. Comp.
Psychol. 113, 426–434. doi: 10.1037/0735-7036.
113.4.426
Rajaram, S. (1993). Remembering and knowing - 2
means of access to the personal past.Mem. Cognit.
21, 89–102. doi: 10.3758/BF03211168
Ranganath, C. (2010). Binding items and contexts:
the cognitive neuroscience of episodic mem-
ory. Curr. Dir. Psychol. Sci. 19, 131–137. doi:
10.1177/0963721410368805
Stewart, P. (1964). Jacobellis v Ohio. US Rep 378, 184.
Suddendorf, T., and Corballis, M. C. (2007). The evo-
lution of foresight: what is mental time travel,
and is it unique to humans? Behav. Brain Sci. 30,
299–313. doi: 10.1017/S0140525X07001975
Sutton, J. E., and Shettleworth, S. J. (2008). Memory
without awareness: pigeons do not show
metamemory in delayed matching to sample.
J. Exp. Psychol. Anim. Behav. Process. 34, 266–282.
doi: 10.1037/0097-7403.34.2.266
Templer, V. L., and Hampton, R. R. (2013a). Cognitive
mechanisms of memory for order in rhesus mon-
keys (Macaca mulatta). Hippocampus 23, 193–201.
doi: 10.1002/hipo.22082
Templer, V. L., and Hampton, R. R. (2013b). Episodic
memory in nonhuman animals. Curr. Biol. 23,
R801–R806. doi: 10.1016/j.cub.2013.07.016
Tulving, E. (1972). “Episodic and semantic memory,”
in Organisation of Memory, eds E. Tulving and
W. Donaldson (San Diego, CA: Academic Press),
381–403.
Tulving, E. (1984). Precis of elements of episodic
memory. Behav. Brain Sci. 7, 223–238. doi:
10.1017/S0140525X0004440X
Tulving, E. (2001). “The origin of autonoesis in
episodic memory,” The Nature of Remembering:
Essays in Honor of Robert G. Crowder, eds H.
L. Roediger III, J. S. Nairne, I. Neath, and
A. M. Surprenant (Washington, DC: American
Psychological Association), 17–34.
Tulving, E. (2002). EPISODIC MEMORY: from mind
to brain. Annu. Rev. Psychol. 53, 1–25. doi:
10.1146/annurev.psych.53.100901.135114
Tulving, E. (2005). “Episodic memory and auto-
noesis: Uniquely human,” in The Missing
Link in Cognition: Origins of Self-Reflective
Consciousness, eds H. Terrace and J. Metcalfe (New
York, NY: Oxford University Press), 3–56. doi:
10.1093/acprof:oso/9780195161564.003.0001
Zentall, T. R., Clement, T. S., Bhatt, R. S., and Allen, J.
(2001). Episodic-like memory in pigeons. Psychon.
Bull. Rev. 8, 685–690. doi: 10.3758/BF03196204
Zhou, W., Hohmann, A. G., and Crystal, J. D. (2012).
Rats answer an unexpected question after inci-
dental encoding. Curr. Biol. 22, 1149–1153. doi:
10.1016/j.cub.2012.04.040
Conflict of Interest Statement: The author declares
that the research was conducted in the absence of any
commercial or financial relationships that could be
construed as a potential conflict of interest.
Received: 09 January 2015; accepted: 14 January 2015;
published online: 04 February 2015.
Citation: Basile BM (2015) Rats remind us what actu-
ally counts in episodic memory research. Front. Psychol.
6:75. doi: 10.3389/fpsyg.2015.00075
This article was submitted to Comparative Psychology, a
section of the journal Frontiers in Psychology.
Copyright © 2015 Basile. This is an open-access article
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Frontiers in Psychology | Comparative Psychology February 2015 | Volume 6 | Article 75 | 2


Rats remind us what actually counts in episodic memory research

Benjamin M Basile

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