Episodic
memory has been defined as memory of personal events and specific
episodes in one’s life, and it is thought to be linked to self-awareness
[e.g.,
3,
4].
Whether non-human animals possess some forms of episodic memory is a
controversial topic, and it is difficult to design experimental
procedures to assess self-awareness unambiguously. Therefore, this form
of memory in non-human animals is referred to as “episodic-like memory.”
The diversity of methods to investigate episodic-like memory reflects
the controversies regarding its definition [
5,
6,
7,
8];
however, recent approaches seem to agree that the recalling of an event
relies on episodic memory when encoding of such event was incidental [
9,
10,
11,
12,
13].
Incidental encoding occurs when information is stored without knowing
that it has to be remembered or that it will be important later [
9].
This requisite ensures that the subject cannot rely on learned rules
(semantic memory) to succeed in the subsequent memory test. Because, at
present, no experimental procedure exists to directly assess the type of
encoding (i.e., a subjective state), a crucial criterion of studies
focusing on episodic-like memory is that the recall test should be
unexpected [
1].
Unexpectedness of the test ensures that there is no specific motivation
for explicit encoding, so incidental encoding can be reasonably
assumed.
To explore the ability of dogs to recall past
events when there was no expectation of the recall test, we used an
innovative methodology: a modified version of the “Do as I Do” paradigm,
relying on dogs’ ability to imitate human actions after a delay [
14,
15].
Our aim was to test dogs’ episodic-like memory of past events (i.e.,
human actions) that are richer in content and more complex than what was
tested in the majority of previous studies [e.g.,
7,
9,
16,
17].
In most of these studies, laboratory animals were tested on memory of
simple events, such as object exploration or feedings. Although these
findings provide important advances for the study of episodic memory,
real-life events are far more complex and richer in content.
Particularly, from a pet dog’s perspective, the actions of humans are
arbitrary behaviors that are always potentially different and can be
performed on many different objects and in many different contexts.
Episodic-like memory of such context-rich events was not tested
previously in non-human species, except for chimpanzees and orangutans [
5]; thus, it is not known whether this ability evolved only in primates or is a more widespread trait.
Here,
we investigate whether dogs can rely on episodic-like memory to recall
context-rich events from the past. We hypothesized that dogs can rely on
episodic-like-memory to recall and imitate incidentally encoded actions
performed by their owners, and we tested two predictions. First, we
expected dogs to be able to imitate incidentally encoded actions when
the imitation test was unexpected, albeit less successfully compared to
their baseline imitation success when recall is expected. Second, we
predicted that imitation success would decrease significantly with
longer retention intervals, as memory appears to decay faster when
encoding is incidental as opposed to when it is intentional [
7,
18,
19].
Before testing, pet dogs were trained in two stages; the first stage
has been independent of this study, as we enrolled dogs that were
previously trained by their owners with the regular Do as I Do training
to imitate human actions on command “Do it!” [
2,
14] (for more details, see “Do as I Do training” in
Supplemental Experimental Procedures). At the beginning of this study, the dogs’ baseline imitation success was assessed with the two-action method [
20]
in an expected imitation test (“baseline imitation” henceforth). Every
dog had been exposed once to the demonstration of one of two possible
novel (not trained) actions on an object (e.g., climb on a chair or
touch the chair with paws; see
Table S1).
After the demonstration, the owner gave the “Do it!” command. Dogs were
then free to perform any action, including other actions than those
chosen for the tests.
To ensure that the subsequent
imitation test was unexpected, after the baseline test, dogs underwent a
second stage of training in which they were not required to imitate
anymore. Instead, after the owners’ demonstration of various actions in
sessions of six different trials, dogs were always required to perform a
simple training exercise: lying down (“Lie down training” in
Supplemental Experimental Procedures).
The aim of this training was to substitute the dogs’ expectation of the
imitation command with the expectation of a “Lie down” command. After
the successful “Lie down” training, we tested dogs’ memory of unfamiliar
(previously not trained or tested) actions by unexpectedly commanding
them to imitate instead of lying down (
Movie S1).
Dogs were tested with the “Do it!” command only if they lied down
spontaneously after the demonstration, suggesting with their behavior
that they expected a lie down command (all dogs lied down
spontaneously).
Dogs were not allowed to motor practice
the demonstrated actions; they could only observe them during the
demonstration. We tested each dog in two imitation tests: after
retention intervals (i.e., time between demonstration and the “Do it!”
command to imitate) of 1 min and 1 hr, in random order of the delays and
the demonstrated actions. The tests were video recorded and later
behaviorally coded for statistical analysis. It is reasonable to assume
that in these tests, a successful imitation of the previously
demonstrated action was possible only if dogs encoded the action
incidentally, because the imitation test was unexpected, so there was no
motivation for the dogs to encode them explicitly. Therefore, our
method complies with the requirements for testing episodic memory
(recall of an incidentally encoded event assessed by an unexpected
recall test).
The unexpectedness of the test is a
critical and at the same time challenging issue because it is difficult
to assess the mental state of non-verbal subjects (i.e., acquire
information about their expectations). Previous studies relied on the
mere assumption that the test was unexpected [
5,
9,
10,
11,
12,
13].
In contrast, we experimentally modified dogs’ expectations and searched
for behavioral evidence for this. First, we ensured that the dogs
expected to receive the “Lie down” command—and not the imitation
command—by training all dogs until they spontaneously lied down after
they had seen the demonstrated actions in at least five of six trials in
two consecutive training sessions. In the unexpected tests, all dogs
lied down spontaneously after the demonstrated actions, indicating that
they expected a “Lie down” command, not an imitation command. Second, we
relied on the well-established violation of expectation paradigm [e.g.,
21,
22] that has also been successfully used in dogs [
23,
24,
25].
This paradigm predicts a longer duration of looking toward the source
of violation of expectation; therefore, we expected longer duration of
looking at the owner who issued the “Do it!” command when this was
unexpected as opposed to when it was expected. Because of the excess of
zeros in the expected imitation tests (due to dogs that did not look at
the owner after the “Do it!” command was given), we analyzed duration of
looking in Tweedie Generalized Linear Mixed Models (GLMMs; package
“cplm” [
26] in R statistical environment, v. 3.2.3 [
27]),
with dog ID as random term and test condition as fixed effect (factor
with three levels: baseline [expected imitation test], 1 min [unexpected
imitation test], and 1 hr [unexpected imitation test]). Dogs looked
significantly longer at the owner in the two conditions with unexpected
imitation test than in the baseline condition with expected imitation
test (likelihood ratio test of Tweedie GLMMs with and without test
condition as fixed factor: χ
22 = 25.45, p < 0.001;
Figure 1).
Other than expectedness, longer duration of looking may be explained by
between-group differences in retention times and the effect of
distraction by the “Lie down” command. Therefore, we excluded these
alternative explanations in further analyses comparing the duration of
looking in the present study with that of previous studies with
identical delays but expected imitation tests (
Figure 1 and “Violation of expectation” analysis in
Supplemental Experimental Procedures).
Imitation success (binary response variable) was analyzed using binomial GLMMs (R package “lme4” [
27]),
with dog ID as random term and test condition as fixed effect (factor
with three levels: baseline [expected imitation test], 1 min [unexpected
imitation test], and 1 hr [unexpected imitation test]). In support of
both of our predictions, we found that dogs were able to imitate when
the imitation test was unexpected (although less successfully than when
it was expected), and imitation success decreased quickly (i.e., fewer
subjects imitated) with increasing retention interval (GLMM of imitation
success, effect of test condition: χ
22 = 14.7, p < 0.001;
Table 1;
Figure 2).
A more rapid decay of dogs’ memory as a result of incidental encoding
was apparent when we compared imitation success after 1 min and 1 hr
retention interval when recalling was unexpected (this study) with
results of our previous studies, with similar conditions (also with
1 min and 1 hr retention intervals) but when the imitation test was
expected [
14,
15] (
Figure 2).
When the recall test was expected, imitation success of dogs was not
significantly different between immediate recall and recall after 1 hr
delay [
15].
In addition, imitation success with expected recall was more than
2-fold compared to when recall was unexpected (binomial GLM of imitation
success after 1 hr retention intervals, expected recall [from 15]
versus unexpected recall [this study]: 83.3% versus 35.3%; χ
21 = 7.0, p = 0.008, regression coefficient [B ± SE] for expectedness = 2.22 ± 0.93).
Table 1Imitation Success
| Effects of Test Condition | Parameter Estimate ± SE | z | p |
|---|
| Intercept (baseline, expected) | 2.87 ± 1.11 | 2.59 | 0.010 |
| Baseline (expected) → 1 min (unexpected) | −2.50 ± 1.19 | −2.10 | 0.036 |
| Baseline (expected) → 1 hr (unexpected) | −3.51 ± 1.27 | −2.77 | 0.006 |
We argue that the difference in memory decay between this study and the previous one with identical delay [
15]
further corroborates that the dogs relied on an episodic-like memory in
the present study, as this type of memory is proposed to decay faster
with time than other types of long-term memory [
18,
19].
In the case of expected imitation tests, dogs may have encoded the
owners’ demonstrated actions explicitly because, as a result of previous
training, they expected to be required to imitate. This implies that
dogs might have used semantic memory to succeed in the deferred
imitation task. In contrast, in the present study dogs were tested in
the deferred imitation test only after assuring that their expectation
of the future action required from them was different from the
demonstrated action. Despite this, our results suggest that dogs could
encode the demonstrated actions incidentally, although less successfully
compared to the baseline.
Ostensive signals used by the
owners to prevent dogs from moving during the demonstrations (“Stay and
pay attention” command) may have increased the dogs’ attention, but this
is unlikely to have resulted in using explicit memory in the unexpected
tests. The same cues were also used during the “Lie down” training, in
which dogs specifically learned that the owner’s subsequent actions were
irrelevant. In addition, this command is commonly used in everyday life
situations with pet dogs, whenever owners want to prevent their dogs
from interfering with their activities. Following the concept of
incidental encoding (not knowing that the information will be important
later [
1,
9]),
we experimentally modified dogs’ expectations so that recalling the
previously demonstrated actions was unexpectedly required. Although we
provided multiple, independent experimental evidence for unexpectedness
of recall (spontaneous lying down at the beginning of the test and
behavioral signs of violation of expectation when unexpectedly required
to imitate), we acknowledge that ensuring incidental encoding by direct
evidence is problematic because it concerns the inner state of the
subjects. Such direct and exclusive evidence seems extremely challenging
to provide (if not impossible), so we relied on the assumption that the
“Lie down” training resulted in dogs not explicitly encoding the
demonstrated actions because these were irrelevant for the subsequent
task. A steeper decrease in imitation success, albeit as an indirect
evidence, strongly supports that we succeeded in this [
18,
19].
Importantly,
by using the two-action procedure in which two actions (A or B) are
demonstrated on an object, our study provides evidence that the
underlying process resulting in dogs’ reproduction of the demonstrated
actions was deferred imitation (in 94.3% of all the tests when dogs
performed action A or B, it was in correspondence with the demonstrated
actions;
Table 2; see
Supplemental Experimental Procedures
for more details on this analysis). This supports the notion that the
dogs could imitate owners’ actions that were incidentally encoded
without being presented with samples of those at the time of recall and
without motor practicing during the retention interval.
Table 2Imitation Analysis
| Test Condition and Retention Interval | Demonstrated A | Demonstrated B |
|---|
| Performed A | Performed B | Performed Other | Performed A | Performed B | Performed Other |
|---|
| Baseline imitation | 9 | 0 | 1 | 0 | 7 | 0 |
| 1 min unexpected | 5 | 1 | 2 | 0 | 6 | 3 |
| 1 hr unexpected | 5 | 0 | 5 | 1 | 1 | 5 |
Testing for deferred
imitation is a widely used approach to investigate the development of
cognitive abilities in human infants [e.g.,
28] and chimpanzees [
29,
30].
These studies, however, were not specifically designed to investigate
episodic memory, and it cannot be determined whether encoding of the
demonstrations was incidental. Incidental encoding may also occur in
cases of latent learning [
31],
although it has to be confirmed. Important advances about recall of
incidentally acquired information were recently made by authors applying
methods that rely on the unexpectedness of the recall test [
9,
10,
11,
12,
13]. Zentall et al. [
11]
argued that in order to investigate episodic-like memory in non-verbal
species, it is possible to teach them to use a trained behavioral
response to “answer” a question about a past event (e.g., “Did you peck
or not?”). Then the subjects can be “asked” this question unexpectedly,
to assess whether they can remember the event. Using this method, the
authors provided evidence that pigeons recall a simple species-specific
action (pecking) and its location [
12] after short delays. Zhou et al. [
9]
revealed that rats could not solve an unexpected memory task when the
CA3 region of their hippocampus was inactivated, suggesting that this
brain region is involved when recalling from memory is unexpected.
Martin-Ordas et al. [
5]
tested chimpanzees and orangutans on their ability to recall the
location of tools that they used previously to retrieve food. This study
showed the ability to recall tool locations for long delays—even 3
years—after having used them. Although this suggests that some non-human
species may recall events with a more complex nature than those tested
in previous studies, the role of previous motor practice cannot be
completely excluded due to the fact that those subjects performed the
actions before testing. Mercado et al. [
32]
tested dolphins on their ability to reproduce the action they had just
performed. Although, given the short delay, the subjects could have
relied on their working memory, this methodological approach has the
potential to test episodic-like memory for complex past events (one’s
own actions) if subjects are prevented from keeping their mind actively
on the actions so that the unexpectedness of the test can be ensured.
Our
study makes an important advance in the study of episodic-like memory
for multiple reasons. To our knowledge, this is the first time that a
non-human species shows evidence of being able to recall complex events
(i.e., others’ actions) without motor practicing on them during the
retention interval—thus relying on a mental representation of the action
that has been formed during incidental encoding, as assessed by an
unexpected test. Note that in most previous studies of episodic-like
memory, subjects participated in sample trials in which the same stimuli
were presented as in test trials [e.g.,
16,
17].
Our experimental procedure ensured that even if dogs were presented at
the time of the test with the same objects that were used at the time of
encoding, the specific actions performed by the demonstrator could only
be imitated if dogs recalled a mental representation that was formed
during encoding.
This modified version of the Do as I Do
method has the potential to be applicable to a variety of species; the
list of species in which the Do as I Do method has been used
successfully includes dolphins (
Tursiops truncatus) [
33], parrots (
Psittaciformes) [
34], and killer whales (
Orcinus orca) [
35].
Moreover,
to our knowledge this is the first study that experimentally addressed
and behaviorally confirmed unexpectedness of the recall test. We believe
that our research approach of modified expectation combined with the
violation of expectation paradigm can be adapted to various experimental
designs.
In conclusion, by using a modified version of
the Do as I Do method, we found evidence that dogs can remember events
as complex as human actions after incidental encoding, as assessed by an
unexpected memory test, without motor practicing the actions during the
retention interval and without being presented at the time of the
memory test with the same samples presented when encoding took place.
This is the first evidence of episodic-like memory of others’ actions in
a non-human species, and it is the first report of this type of memory
in dogs. We suggest that dogs might provide a new non-human animal model
to study the complexity of incidental encoding of context-rich events,
especially because of their evolutionary and developmental advantage to
live in human social groups.
Article Info
