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Metacognition in Animals

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Abstract

Metacognition is thinking about thinking. There is considerable interest in developing animal models of metacognition to provide insight about the evolution of mind and a basis for investigating neurobiological mechanisms of cognitive impairments in people. Formal modeling of low-level (i.e., alternative) mechanisms has recently demonstrated that prevailing standards for documenting metacognition are inadequate. Indeed, low-level mechanisms are sufficient to explain data from existing methods. Consequently, an assessment of what is 'lost' (in terms of existing methods and data) necessitates the development of new, innovative methods for metacognition. Development of new methods may prompt the establishment of new standards for documenting metacognition.
Metacognition in Animals 1
Metacognition in animals
Jonathon D. Crystal & Allison L. Foote
University of Georgia
Metacognition is thinking about thinking. There is considerable interest in developing animal models of metacognition to
provide insight about the evolution of mind and a basis for investigating neurobiological mechanisms of cognitive impair-
ments in people. Formal modeling of low-level (i.e., alternative) mechanisms has recently demonstrated that prevailing
standards for documenting metacognition are inadequate. Indeed, low-level mechanisms are sufcient to explain data from
existing methods. Consequently, an assessment of what is ‘lost’ (in terms of existing methods and data) necessitates the
development of new, innovative methods for metacognition. Development of new methods may prompt the establishment
of new standards for documenting metacognition.
Keywords: Metacognition, comparative metacognition, uncertainty monitoring, metamemory, quantitative modeling.
A dening feature of human existence is the ability to re-
ect on one’s own mental processes, termed metacognition
(Descartes, 1637; Metcalfe & Kober, 2005). Consequently,
a fundamental question in comparative cognition is whether
nonhuman animals (henceforth animals) have knowledge
of their own cognitive states (Smith, Shields, & Washburn,
2003). Answering this question not only provides critical
information about the evolution of mind (Emery & Clayton,
2001), but also provides a potential framework for investi-
gating the neurobiological basis of cognitive impairments in
people (Hoerold et al., 2008; Robinson, Hertzog, & Dun-
losky, 2006; Shimamura & Metcalfe, 1994).
The presentation of a stimulus gives rise to an internal rep-
resentation of that stimulus (which is referred to as the pri-
mary representation). Primary representations are the basis
for many behaviors. For example, when presented with an
item on a memory test, it is possible to evaluate familiar-
ity with the item to render a judgment that the item is new
or old. Metacognition involves a secondary representation
which operates on a primary representation. For example,
a person might know that he does not know the answer to a
question, in which case appropriate actions might be taken
(such as deferring until additional information is available).
To document metacognition, we need a method that assigns
performance to the secondary representation (i.e., we need
to be certain that performance is not based on the primary
representation).
Carruthers (2008) distinguishes between rst-order ex-
planations and metacognition. First-order explanations are
“world-directed” rather than “self-directed” according to
Carruthers. According to this view, rst-order explanations
are representations about stimuli in the world (i.e., beliefs
about the world), whereas metacognition involves represen-
tations about beliefs (i.e., knowing that you hold a particu-
lar belief). Note that according to the denition provided
above, metacognition involves knowledge about one’s cog-
nitive state. Thus, a variety of other conditional arrange-
ments would not constitute metacognition. For example,
discriminating an internal, physiological state would not
constitute metacognition. Similarly, discriminating hierar-
chical relations between a variety of stimuli and responses
(e.g., occasion setting) would not constitute metacognition.
Carruthers argues that putative metacognitive phenomena in
animals may be explained in rst-order terms
1
.
With human participants, we can ask people to report
about their subjective experiences using language. Self
Jonathon D. Crystal and Allison L. Foote, Department of Psy-
chology, University of Georgia, Athens GA 30602-3013
This work was supported by National Institute of Mental
Health grant R01MH080052 to JDC. The content is solely the
responsibility of the authors and does not necessarily represent
the ofcial views of the National Institute of Mental Health or
the National Institutes of Health. Correspondence concerning
this article should be addressed to JDC at jcrystal@uga.edu.
Volume 4, pp 1 -16
2009
ISSN: 1911-4745 doi: 10.3819/ccbr.2009.40001 © Jonathon D. Crystal 2009
Metacognition in Animals 2
reports of subjective experiences play a prominent role in
investigations of metacognition in people (Nelson, 1996).
Although these reports may not be perfect, they provide a
source of information that is not available from nonverbal
animals. Consequently, the difcult problem of assessing
metacognition in animals requires the development of be-
havioral techniques from which we may infer the existence
of metacognition. A frequent approach is to investigate the
possibility that an animal knows when it does not know the
answer to a question; in such a situation, an animal with
metacognition would be expected to decline to take a test,
particularly if some alternative, desirable outcome is avail-
able. Importantly, it is necessary to rule out simpler, alterna-
tive explanations. In particular, we need to determine that
the putative case of metacognition is based on a secondary
representation rather than on a primary representation. For
example, if principles of associative learning or habit for-
mation operating on a primary representation may account
for putative metacognition data, then it would be inappropri-
ate to explain such data based on metacognition (i.e., based
on a secondary representation); the burden of proof favors
primary representations, by application of Morgan’s canon
(Morgan, 1906). We shall refer to explanations that apply
primary representations without appeal to secondary rep-
resentations as simpler or low-level alternative hypotheses
to metacognition. Such considerations raise the question of
the standards by which putative metacognition data are to
be judged. A standard species criteria that must be met to
infer metacognition using methods that cannot be explained
by simpler, alternative hypotheses. We recognize that the
details of an alternative hypothesis need to be specic (and
specication is provided below), but it is worth recognizing
that alternatives to metacognition are simpler (i.e., only pri-
mary representations are required). We also note that use of
a complex experimental task does not imply that data from
such a task require a complex explanation (e.g., a secondary
representation). From our perspective, the main issue is the
appropriateness of appealing to a complex proposal. Thus,
the purpose of testing a less complex proposal is to deter-
mine if the output of the low-level model can account for the
data. If the output of the model accounts for the data, then
it is not appropriate to select the more complex proposal to
explain the data (absent an independent line of evidence that
cannot be explained by the low-level model). Thus, it is ill-
advised to choose to not apply the low-level model because
of claims that the primary task is sophisticated, especially
if the low-level model can produce the observed pattern of
data.
It has long been recognized that an animal might learn to
decline difcult tests by discriminating the external stimuli
that are associated with such tests (Inman & Shettleworth,
1999); we refer to this class of explanations as a stimulus-
response hypothesis (i.e., in the presence of a particular
stimulus, do a specic response). Consequently, an impor-
tant standard by which to judge putative metacognition data
emerged (Inman & Shettleworth, 1999), according to which
task accuracy provided an independent line of evidence for
metacognition.
The goal of this article is to apply low-level explanations
of putative metacognition data to a broad series of experi-
ments in this domain. We nd that existing experiments on
uncertainty monitoring can be explained by low-level expla-
nations without assuming metacognition.
Predictions about task accuracy
An inuential article by Inman and Shettleworth (1999)
introduced the idea that it is critical to assess accuracy with
and without the opportunity to decline difcult tests. They
argued that an animal without metacognition would have the
same level of accuracy when tested with and without the op-
portunity to decline tests (we note that this hypothesis has
recently been challenged by quantitative modeling (Smith,
Beran, Couchman, & Coutinho, 2008), as discussed below).
Inman and Shettleworth hypothesized that an animal with
metacognition should have higher accuracy when it chooses
to take a test compared with accuracy when it is forced to
take the test. The rationale for this hypothesis follows: If the
animal ‘knows that it does not know’ the correct response,
then it will decline the test; moreover, being forced to take
a test is likely to degrade performance because forced tests
include trials that would have been declined had that option
been available.
Thus, the prevailing standard since Inman and Shettleworth
(1999) includes two criteria: (1) the frequency of declining a
test should increase with the difculty of the task and (2) ac-
curacy should be higher on trials in which a subject chooses
to take the test compared with forced tests, and this accuracy
difference should increase as task difculty increases (we
refer to this latter pattern as the Chosen-Forced performance
advantage). Inman and Shettleworth also emphasized that it
is necessary to impose the choice to take or decline the test
before being presented with the test.
Representative data
We show two examples of data that meet the prevailing
standard, from a rhesus monkey (Macaca mulatta) (Hamp-
ton, 2001) and rats (Rattus norvegicus) (Foote & Crystal,
2007). Hampton (2001) used daily sets of four clip-art im-
ages in a matching to sample procedure (i.e., reward was
contingent on selecting the most recently seen image from a
set of distracter images). The procedure is outlined in Figure
Metacognition in Animals 3
Study
Phase
Delay
Interval
Choice
Phase
Test Phase
or Small
Reward
Delay
p=0.33 p=0.67
Preferred
Peanut
If Correct
Primate
Pellet
0
0.2
12.5 25 50
Delay (s)
p(Correct or Declined)
100 200
0.4
0.6
0.8
1
A
B
Figure 1. Schematic representation of design of study and data. Procedure for monkeys (left panel; Hampton, 2001): After
presentation of a clip-art image to study and a retention-interval delay, a choice phase provided an opportunity for taking or
declining a memory test; declining the test produced a guaranteed but less preferred reward than was earned if the test was
selected and answered correctly (test phase); no food was presented when a distracter image was selected in the memory
test. Items were selected by contacting a touch-sensitive computer monitor. Data (right side; Hampton, 2001): Perfor-
mance from a monkey that both used the decline response to avoid difcult problems (i.e., relatively long retention intervals)
and had a Chosen-Forced performance advantage that emerged as a function of task difculty (i.e., accuracy was higher on
trials in which the monkey chose to take the test compared with forced tests, particularly for difcult tests). Filled squares
represent the proportion of trials declined, and lled and unlled circles represent proportion correct on forced and chosen
trials, respectively. Error bars represent standard errors. (Adapted from Hampton, R. (2001). Rhesus monkeys know when
they remember. Proceedings of the National Academy of Sciences of the United States of America, 98, 5359-5362. © 2001
The National Academy of Sciences. Reprinted with permission.)
Metacognition in Animals 4
Figure 2. Procedure for rats (top left panel; Foote & Crystal, 2007): After presentation of a brief noise (2-8 s; study phase),
a choice phase provided an opportunity for taking or declining a duration test; declining the test produced a guaranteed but
smaller reward than was earned if the test was selected and answered correctly (test phase). The yellow shading indicates
an illuminated nose-poke (NP) aperture, used to decline or accept the test. Data (Foote & Crystal, 2007): Performance
from three rats (bottom panels) and the mean across rats (top-middle and top-right panels). Difcult tests were declined
more frequently than easy tests; difculty was dened by proximity of the stimulus duration to the subjective middle of the
shortest and longest durations). The decline in accuracy as a function of stimulus difculty was more pronounced when
tests could not be declined (forced test) compared to tests that could have been declined (choice test). Error bars represent
standard errors. (Adapted from Foote, A. L., & Crystal, J. D. (2007). Metacognition in the rat. Current Biology, 17, 551-
555. © 2007 by Elsevier Ltd.)
Study
Phase
2- 8 s
p=0.33
Choice
Phase
Test Phase
or Small
Reward
Left
NP
Take
6 pellets if correct lever
0 pellets if incorrect lever
3 pellets
Test
Left Lever
p=0.67
Left
NP
Right
NP
Decline Test
Right Lever
Head Entry
into Food
Trough
0.0
0.2
0.1
2.25 2.00
Index of Stimulus Difficulty
Mean
Proportion of Tests Declined
1001.75 1.50 1.25
0.3
0.4
0.5
0.0
0.25
2.25 2.00
Mean
Choice Test
Forced Test
Proportion Correct
1001.75 1.50 1.25
0.50
0.75
1.00
Index of Stimulus Difficulty
Proportion of Tests Declined
0.0
0.05
2.25 2.00 1001.75 1.50 1.25
0.10
0.15
0.20
2.25 2.00 1.001.75 1.50 1.25
0.0
0.2
0.4
0.6
0.8
2.25 2.00 1.001.75 1.50 1.25
0.0
0.2
0.4
0.6
2.25 2.00 1001.75 1.50 1.25
0.0
0.25
0.50
0.75
1.00
2.25 2.00 1.001.75 1.50 1.25
0.0
0.25
0.50
0.75
1.00
2.25 2.00 1.001.75 1.50 1.25
0.0
0.25
0.50
0.75
1.00
Choice Test
Forced Test
Rat1 Rat 2 Rat 3
Proportion Correct
Rat1 Rat 2 Rat 3
A
B
Metacognition in Animals 5
1. Foote and Crystal (2007) presented a noise from a set of
eight durations, which was to be categorized as short or long
(i.e., reward was contingent on judging the four shortest and
four longest durations as short and long, respectively). The
procedure is outlined in Figure 2. The two experiments had
the following common features. Before taking the test, the
animals were given the opportunity to decline it. On other
trials, the animals were not given the option to decline the
test. Accurate performance on the test yielded a valuable
reward, whereas inaccurate performance resulted in no re-
ward. Declining a test yielded a less valuable but guaranteed
reward. The decline rate increased as a function of difculty
(longer retention intervals for the monkey or proximity to
the subjective middle of short and long durations for the rats)
and accuracy was lowest on difcult tests that could not be
declined. Note that the data in Figures 1 and 2 meet the pre-
vailing standard: not only did the animals appear to use the
decline response to avoid difcult problems, but the Chosen-
Forced performance advantage emerged as a function of task
difculty.
Quantitative modeling
Recent quantitative modeling by Smith and colleagues
(2008) shows that low-level (i.e., alternative) mechanisms
can produce both apparently functional use of the decline
response and the Chosen-Forced performance advantage;
these alternatives are low level in the sense that they use
primary representations without application of secondary
representations. Consequently, the formal modeling sug-
gests that the prevailing standard is inadequate to document
metacognition.
Smith and colleagues used basic associative and habit
formation principles in their quantitative model. They pro-
posed that direct reward of the decline response produces a
low-frequency tendency to select that response independent
of the stimulus in the primary discrimination
2
. We note that
Smith et al proposed that the decline response has a constant
attractiveness across the stimulus continuum; constant at-
tractiveness means that the tendency to produce the response
is constant across stimulus conditions. We refer to this class
of threshold explanations as a stimulus-independent hypoth-
esis to contrast it with the stimulus-response hypothesis out-
lined above (the explanatory power of a stimulus-indepen-
dent hypothesis will be evaluated below). For the primary
discrimination, Smith et al. used standard assumptions about
exponential decay of a stimulus (i.e., generalization decre-
ments for an anchor stimulus in a trained discrimination);
exponential decay is also commonly used to model a fading
memory trace (Anderson, 2001; Killeen, 2001; Sargisson &
White, 2001, 2003, 2007; Shepard, 1961; Sikström, 1999;
White, 2001, 2002; Wixted, 2004). Such exponential decay
functions have extensive empirical and theoretical support
(Shepard, 1961, 1987; White, 2002). Thus, the primary dis
-
crimination and the decline option give rise to competing re-
sponse-strength tendencies, and Smith et al. proposed a win-
ner-take-all response rule (i.e., the behavioral response on a
given trial is the one with the highest response strength). A
schematic of the formal model appears in Figure 3a. Sim-
ulations with this quantitative model document that it can
produce both aspects of the prevailing standard (Figure 3b):
the decline response effectively avoids difcult problems,
and the Chosen-Forced performance advantage emerges as a
function of task difculty. Note that both empirical aspects
of putative metacognition data are produced by the simula-
tion (Figure 3b) without the need to propose that the animal
‘knows when it does not know’ or any other metacognitive
process.
Our goal is to assess the impact of applying Smith and
colleagues’ (2008) model depicted in Figure 3a to a broad
set of experiments on metacognition. In our view, it is im-
portant to note that the modeling generates predictions that
are stimulus independent in contrast to the traditional stimu-
lus-response hypothesis. According to a stimulus-response
hypothesis, an animal is assumed to learn to do a particular
response in the presence of a particular stimulus. For ex-
ample, with a stimulus response mechanism, an animal can
learn to do a particular response (such as a decline response)
in particular stimulus conditions at a higher rate than in oth-
er stimulus conditions; such a stimulus-response hypothesis
would take the form of an inverted U-shaped function in Fig-
ure 3a for the decline response (i.e., replacing the constant
attractiveness proposed by Smith et al.’s threshold in Figure
3a). By contrast, according to a stimulus-independent hy-
pothesis, previous reinforcement with a particular response
is sufcient to produce that response in the future at a rela-
tively low frequency. Note that the response has a constant
attractiveness independent of stimulus context. Our applica-
tion of the ideas described above suggests that many studies
in metacognition are well equipped to test stimulus-response
hypotheses, but are not adequate to test the stimulus-inde-
pendent hypothesis (the details to support this conclusion
appear below).
We emphasize at the outset that our view is not that stim-
ulus-response learning is absent in these types of experi-
ments; indeed, stimulus-response learning is likely at work,
meaning that principles of generalization of training stimuli
to new stimulus conditions are at work too, in addition to
stimulus-independent factors. It is also worth emphasizing
at the outset, that Smith et al. (2008) did not propose that
animals would learn a stimulus-independent use of a decline
response in all experiments. However, they did empha-
size that a history of reinforcement is sufcient to establish
a low-frequency threshold that is independent of stimulus
conditions. Thus, our goal is to evaluate the implications of
Metacognition in Animals 6
the stimulus-independent hypothesis and to determine how
much of the existing data can be explained by applying the
stimulus-independent hypothesis to established methods of
assessing metacognition in animals.
Assessment of what is ‘lost’
(methods and corresponding data)
Formal modeling of low-level alternative mechanisms
that account for putative metacognition data necessitates an
assessment of what is ‘lost’ in terms of existing methods and
data. In our assessment, data from existing methods do not
withstand the scrutiny of the formal modeling. We believe
that recognizing that existing methods are inadequate repre-
sents progress. One potential benet of such an assessment
is that it may lead to the development of new methods to
examine metacognition that are not subject to low-level ex-
planations.
The methods and data shown in Figures 1 and 2 are sub-
ject to modeling by low-level explanations. Indeed, the
schematic in Figure 3 was designed to specically explain
the rat data in Figure 2 (Foote & Crystal, 2007). We agree
that the formal model of Smith et al. (2008) applies to our
data from rats (throughout the remainder of this article we
focus primarily on data from rhesus monkeys because these
are the most extensive and thorough tests of comparative
metacognition). However, in our view, the formal situa-
tion is essentially the same for the monkey data in Figure 1
(Hampton, 2001). We outline the formal situation in Figure
4. In the case of delayed-matching to sample, we may as-
sume that the presentation of a sample stimulus gives rise to
a fading memory trace after stimulus termination (Anderson,
2001; Killeen, 2001; Sargisson & White, 2001, 2003, 2007;
Shepard, 1961; Sikström, 1999; White, 2001, 2002; Wixted,
2004). Thus, the horizontal axis in Figure 3 could be repre-
sented as trace decay, which grows as a function of retention
interval (i.e., the independent variable in Hampton’s study).
A low-frequency threshold is used for the decline response.
Smith and colleagues’ simulations suggest that this type of
model can produce both apparently functional use of the
decline response to avoid difcult problems and a Chosen-
Forced performance advantage that emerges as a function of
task difculty.
Metamemory
The case of memory is less perceptually grounded than
temporal discrimination, and it may be argued that memory
is more abstract or sophisticated. However, we believe that
it is possible to apply the formal model by using a trace-de-
cay continuum for a fading stimulus trace. Thus the model
may be sufcient to explain the decline rate and the Chosen-
0
0.2
0 20 40
Objective Level
Threshold
Threshold
LongShort
Forced
Response Proportion
60 80
0.4
0.6
0.8
1
B
0
0.2
0 20 40
Subjective Level
Response Strength
60 80
0.4
0.6
0.8
1
A
Figure 3. Schematic of low-level, response-strength model
and simulation. (a) Presentation of a stimulus gives rise to
a subjective level or impression of that stimulus. For any
given subjective level, each response has a hypothetical re-
sponse strength. The schematic outlines response strengths
for two primary responses in a two-alternative forced-choice
procedure and for a third (i.e., decline or uncertainty) re-
sponse (labeled threshold). Note that response strength is
constant for the third response (i.e., it is stimulus indepen-
dent). By contrast, response strength is highest for the easi-
est problems (i.e., the extreme subjective levels). Note also
that for the most difcult problems (i.e., middle subjective
levels) the decline-response strength is higher than the other
response strengths. Reproduced from Smith et al. (2008).
(b) Simulation of schematic shown in (a). Simulation of a
response-strength model with a at threshold produces ap-
parently functional use of the decline response (i.e., inter-
mediate, difcult stimuli are declined more frequently than
easier stimuli). The Choice-Forced performance advantage
emerges as a function of stimulus difculty. Reproduced
from Smith et al. (2008). (From Smith, J. D., Beran, M. J.,
Couchman, J. J., & Coutinho, M. V. C. (2008). The com-
parative study of
Metacognition in Animals 7
Forced performance advantage. In particular, it is possible
that the monkey’s performance depicted in Figure 1 could
be based on a primary representation of trace strength. Ac-
cording to this view, use of the decline response is based on a
fading memory trace just as the old-new responses from the
primary task are based on a fading memory trace. Because
the same fading memory trace (i.e., the same primary repre-
sentation) is used for both the primary memory task and the
decline response, it is not clear that a secondary representa-
tion is needed to explain the data. The use of two differ-
ent responses (decline and matching responses) does not, in
itself, indicate that the two responses are based on different
types of representations, as outlined next.
The interpretive problem here is how to determine if the
monkey is responding on the basis of a primary represen-
tation (i.e., the strength of stimulus representation is very
weak) or on the basis of a secondary representation (i.e., the
monkey knows that it does not know the correct answer). It
is not sufcient to claim that any paradigm that uses memory
as the primary task will, by denition, result in secondary
representations about memory (and thus, by denition, con-
stitute evidence for metamemory). What data specically
implicates the use of a secondary representation? Before
Smith and colleagues documented putative metacognitive
data patterns based on low-level mechanisms, the answer to
this question was that the Chosen-Forced performance ad-
vantage could not be explained without appeal to metacogni-
tion. However, this pattern of data is not as informative as
previously supposed. The burden of proof, in this situation,
is on providing evidence that implicates a secondary repre-
sentation, and until such evidence is provided the cautious
interpretation is to claim that a primary representation is suf-
cient to explain the data. We also note that the observation
that the memory trace is an internal representation is not ad-
equate to answer the question posed above. Indeed, all rep-
resentations are internal. If all that is needed is an internal
representation (what we have been referring to as a primary
representation), then what is to prevent the assertion that
performance on matching to sample is based on metacogni-
tion (i.e., a secondary representation)? There are multiple
responses in these types of experiment (i.e., the decline re-
sponse and the primary response of choosing a correct/incor-
rect choice in matching to sample). Thus, it may be argued
that the decline response is dedicated to reporting about a
secondary representation, whereas the other responses are
dedicated to reporting about the primary representation. But
how do we know if this is the case? Clearly, what is needed
is an independent line of evidence. In any case, Smith et al.’s
(2008) model deals very nicely with competition between
responses (i.e., the model successfully picks responses based
on low-level mechanisms without application of a secondary
representation).
Hampton’s (2001) study had several elegant features,
and several of these features were included in a series of
recent elegant tests with pigeons (Sutton & Shettleworth,
2008). For example, after training with one retention inter-
val, Hampton’s monkeys received a novel probe in which no
sample stimulus was presented. This is a direct manipula-
tion of memory, and it is intuitive that an animal with meta-
cognition would respond adaptively by declining the test
(this is what the monkeys did). However, this could also
be based on the primary representation. Indeed, if a sample
is omitted on a probe trial, the trace strength from the most
recently presented sample (i.e., the one presented on the trial
that preceded the probe) would have had a very long time
to decay. In such a situation, the trace strength from the
primary representation would be very low, in which case it
would likely be lower than the threshold for declining the
test. Thus, a decline response would be expected based on
the primary representation. Again, the interpretive problem
here is how to know if the monkey is responding on the ba-
sis of a primary representation (i.e., the strength of stimulus
representation is very weak) or on the basis of a secondary
representation (i.e., the monkey knows that it does not know
the correct answer – in this case because there is no correct
answer).
Memory response
Decline response
Memory Trace Decay (Retention interval)
Response Strength
Figure 4. Schematic of low-level, response-strength model
of metamemory. Presentation of a stimulus gives rise to
a fading memory trace after stimulus termination. Trace
decay (which is shown on the horizontal axis) grows as a
function of retention interval. A low-frequency threshold is
used for the decline response. Note that response strength is
constant for the decline response. By contrast, memory re-
sponse strength is highest for the shortest retention intervals.
Note that for the most difcult problems (i.e., long retention
intervals) the decline response strength is higher than the
memory response strength. Also note that the horizontal
axis may be viewed as a primary representation (see text for
details).
Metacognition in Animals 8
Pervasiveness of reinforcement of uncertainty responses
Some early experiments on uncertainty used direct rein-
forcement variables to inuence the behavior of the monkeys;
for example, an uncertain response sometimes produced a
hint or identication of the currently correct response (e.g.,
Smith, Shields, Allendoerfer, & Washburn, 1998), a guar-
anteed-win trial (e.g., Shields, Smith, & Washburn, 1997;
Smith, Shields, Schull, & Washburn, 1997), a time-out delay
for over-use of the uncertainty response (e.g., Shields et al.,
1997; Smith et al., 1998; Smith et al., 1997), or food (Hamp-
ton, 2001).
Smith and colleagues (Smith et al., 2008) suggested that a
history of reinforcement associated with the decline response
is responsible for the deployment of low-level alternative
explanations. This observation has led to some creative
attempts to circumvent the role of reinforcement (Beran,
Smith, Redford, & Washburn, 2006; Smith, Beran, Redford,
& Washburn, 2006). However, the functional use of a de-
cline or uncertainty response may be due to the existence of
residual reinforcement variables (see below). Consequently,
the low level threshold from Figure 3 may apply, meaning
that the animal’s uncertainty behavior could be explained by
low-level mechanisms.
Pure uncertainty response. Smith and colleagues suggest
that reinforcement of the uncertainty response is responsible
for the deployment of low-level alternative explanations. In-
deed, this observation represents a signicant hurdle for any
method that employs an uncertainty response. For example,
Beran and colleagues (2006) sought to develop a “pure” un-
certainty response that would not be contaminated by rein-
forcement.
Beran and colleagues (2006) trained monkeys in a numer-
osity discrimination. Between one and nine circles were
presented on a computer screen. When the display had less
or more than a designated center value, the monkeys were re-
warded for using a joystick to move a cursor to an “L” (less)
or “M” (more) on the computer screen, respectively. A wide
range of center values was systematically explored, many
congurations of dots were used across trials, and brightness
was controlled. The uncertainty response was a “?” at the
bottom-center of the screen. Moving the joystick to this po-
sition ended the trial and initiated the next trial. Importantly,
the authors emphasize that this method represents a pure un-
certainty response in the sense that the uncertainty response
was not reinforced by food, information about the correct
answer, or the presentation of an easy next trial. Thus, they
conclude that this was the purest trial-decline response pos-
sible.
However, even this valuable attempt to curtail reinforce-
ment may leave some residual reinforcement in place; thus,
Smith et al.’s low-level explanation may apply in this experi-
ment (using the primary representation of numerosity). The
two rhesus monkeys in this study had previous experience
with an uncertainty response from an earlier study that did
not deploy the purest trial-decline procedure (Shields, Smith,
Guttmannova, & Washburn, 2005; Smith et al., 2006); we
note that the problem is not that the monkeys had successful-
ly used an uncertainty response in a previous task, but rather
that they had received reinforcement in the past. Speci-
cally, the monkeys had been rewarded in the past for moving
the joystick down (which was the response in their study).
Training the monkeys to use the joystick involved requiring
the monkeys to learn to (1) approach a perch to view the
video display, (2) reach through the cage mesh to manipu-
late the joystick below the monitor, (3) move the joystick
so that the cursor on the screen contacted computer-gener-
ated stimuli; the joystick response was rewarded with food
(Rumbaugh, Richardson, Washburn, Savage-Rumbaugh,
& Hopkins, 1989; Shields et al., 2005; Washburn & Rum-
baugh, 1992). A history of reinforcement associated with
moving the joystick down would presumably be sufcient
to generate a low-frequency tendency to select this response.
Smith and colleagues’ model would then apply (a winner-
take-all decision between a low-frequency tendency to move
the joystick down to the “?” vs. selection of the “L” or “M”
responses). The model predicts that “L” or “M” would win
when the number of stimuli is far from the center value,
whereas the uncertain response would win near the center
value; thus, the model predicts an increase in the uncertainty
response for the difcult central numbers even if they are not
explicitly reinforced for making these choices in the current
experiment. Moreover, these monkeys are relatively task
savvy, given that they have a long history of participating
in laboratory tasks with joysticks and moving icons to tar-
get locations in addition to other laboratory tasks. The ef-
ciency benets of using task-savvy subjects means that these
subjects generalize from earlier experiments to the current
experiment. This generalization is not surprising given the
similarity between earlier experiments and a current experi-
ment (e.g., sitting at the experimental perch, observing the
computer display, reaching an arm through the mesh cage,
contacting and moving the joystick, receiving reinforcement
for joystick movements, etc.); all of these factors promote
the use of responses from within their experimental reper-
toire in new experiments, thereby allowing the experiment-
ers to forgoe the extensive training experience that would
otherwise be required if new subjects were tested in each
experiment.
Other valuable features of the task (re-training with new
central values, many different congurations of the circles
on the computer screen, etc.) do not mitigate against that
application of the low-level explanation. In this regard, it
Metacognition in Animals 9
is worth noting that the ability to perform the numerosity
discrimination is presumably based on a primary represen-
tation, and for easy numerical discriminations the response
strengths for “L” or “M” would be higher than the hypoth-
esized low-level threshold for responding down to the “?”.
Moreover, there may have been concurrent reinforcement
because the uncertainty option reduced the delay to rein-
forcement in subsequent trials. Reducing delay to reward is
a reinforcement variable (Carlson, 1970; Kaufman & Baron,
1968; Richardson & Baron, 2008), which could maintain the
low-frequency at threshold for the uncertainty response.
To examine the role of delay to reinforcement in these types
of experiments we conducted a simulation of reinforcement
rate. For the simulation, we used the exact feedback de-
scribed by Beran et al. (2006) for their purest trial-decline
response. On the primary task, a correct response produced
1 food pellet, and an incorrect response did not produce any
food pellets. Critically, in their procedure, an incorrect re-
sponse produced a time out of 20 sec. An uncertainty re-
sponse did not produce food and did not produce a time out.
We used a at uncertainty threshold, as proposed by Smith
et al. (2008). In the simulations, we varied the response
strength for the uncertainty response from 0 to 1 using many
intervening values and held all other aspects of the simu-
lation constant
3
. If delay to reinforcement is not a reward
variable in these studies, then the amount of food per unit
time will be constant as a function of the threshold values in
the simulations. By contrast, if delay to reinforcement func-
tions as a reward variable, then there will be some threshold
parameter for the uncertainty response that maximizes food
per unit time.
Figure 5 shows the results of the simulation. Note that
there is a peak in food per unit time. Thus, it is possible
that a subject in these types of experiments could adjust its
threshold level to maximize food per unit time, and this ad-
justment of the “non-reinforced” uncertainty response is re-
inforced by reduced delay to reinforcement in the overall
procedure. This simulation shows that despite the lack of
direct reward for use of the uncertainty response, there are
residual reinforcement variables at work in these types of
experiments. Thus, the uncertainty response was indirectly
reinforced by increased food rate; application of the Smith
et al. (2008) model would predict use of the uncertainty re-
sponse for the intermediate stimuli. Our simulation is con-
sistent with the hypothesis that there are negative affective
consequences of time outs, which has been veried through
independent approaches (Richardson & Baron, 2008).
In summary, it is important to note that although delay to
reinforcement could occur on a trial with any numerosity
display, it is not necessary to assume uncertainty monitoring
in order to produce apparently functional use of the uncer-
tainty response. First, a previous history of reinforcement
of joystick responses is sufcient to establish a low-frequen-
cy tendency to select the “?”. The “?” response loses to “L”
or “M” because “L” or “M” are high based on training in the
numerosity task, except for the most difcult trials in which
the response strength of “L” and “M” are lower than that of
“?” (which produces a preference for “?” at the most difcult
trials). Second, concurrent reinforcement may maintain the
tendency to select “?” at a low frequency, as suggested by
the simulation described above. Third, training with the pri-
mary task (i.e., changing the central value across phases of
training) is responsible for changing the response gradients
associated with the “L” and “M” responses. Certainly, these
gradients would be modeled as primary representations.
Thus, the movement of the expected high point in the use of
“?” is based on the change in the shape of the response gradi-
ents for “L” and “M” as judged against a relatively constant
low-frequency threshold for “?”.
Any of the above sources of reinforcement may be suf-
cient to apply the low-level threshold from Figure 3,
meaning that the monkey’s uncertainty behavior could be
explained by reinforcement and application of the Smith et
al. (2008) model. We also note that the complexity of the
primary task does not play a role in the application of Smith
et al.’s model. The main issue is the appropriateness of ap-
0
0.00 0.25 0.50
Threshold
Food per minute
0.75 1.00
3
6
9
12
Figure 5. Results of a simulation of reinforcement den-
sity as a function of variation in threshold for the uncer-
tainty response. The simulation used the generalization and
constant-threshold concepts from Smith et al. (2008). Re-
inforcement and delays were based on Beran et al. (2006).
Although no food was delivered upon selecting the uncer-
tainty response, the simulation shows that the value of the
threshold for selecting the uncertainty response inuences
the amount of food obtained per unit time in the primary dis-
crimination. Thus, the uncertainty response was indirectly
reinforced despite efforts to eliminate reinforcement.
Metacognition in Animals 10
pealing to a complex proposal (i.e., metacognition). Thus,
the purpose of testing a less complex proposal (i.e., Smith et
al.’s response strength model) is to determine if the output
of the model can account for the data. If the output of the
model accounts for the data, then it is not appropriate to se-
lect the more complex proposal to explain the data (absent
an independent line of evidence that cannot be explained by
the low-level model). It is ill-advised to choose to not ap-
ply the low-level model because of claims that the primary
task is sophisticated, especially if the low-level model can
produce the observed pattern of data.
Trial-by-trail feedback. Another example of the dif-
culty encountered in overcoming the low-level explanations
comes from a recent study by Smith and colleagues (Smith
et al., 2006). In this uncertainty monitoring study, trial-by-
trial feedback was delayed and uncoupled from the respons-
es that earned the feedback. In particular, the monkeys were
presented with a computer display that had a variable num-
ber of randomly placed pixels. Some displays were sparse
and others were dense. The monkeys were required to use a
joystick to move a cursor to an “S” (sparse) or “D” (dense)
on the screen. A “?” appeared at the bottom-center, to be se-
lected for the uncertainty response. As the trials progressed,
the monkeys earned food rewards or 20-s penalties (i.e., a
time-out with a buzzer sound) based on correct or incorrect
responses, respectively. However, the earned rewards or
penalties were not delivered at the end of each trial. Instead,
these consequences were delayed until the completion of a
block of four trials. To further uncouple consequences from
the responses that earned them, the feedback was not pre-
sented in the order in which they were earned. Instead, when
the block ended, all rewards were presented rst, followed
by all time outs. The proportion of “S” and “D” responses
tracked the density of the stimuli and declined toward the
central value. The use of the “?” response peaked near the
central value for one of the monkeys.
This is a highly innovative method to uncouple feedback
in the density discrimination from the specic stimuli that
were present when the feedback was earned, which likely
has many applications. Indeed, it is very impressive that
monkeys learned the task contingencies under these cir-
cumstances. Moreover, there were many other admirable
features of the design (e.g., the monkeys initially received
blocks of one trial – meaning transparent feedback – but the
critical data was subsequently collected using different den-
sity ranges). The central question for our purpose is what
can be predicted from Smith et al.’s (2008) model.
The study employed monkeys with previous reinforce-
ment of the joystick response, so their history of reinforce-
ment could contribute to a low-threshold tendency to select
that option. A history of reinforcement with moving the joy-
stick down may be sufcient to generate a low-frequency
tendency to do this response in the future as discussed above.
The rest of the work is done by the response strengths for the
“S” and “D” options. Because the proportion of “S” and
“D” responses tracked the density of the stimuli, we may
conclude that the animals had lower response tendencies for
“S” and “D” near the central value based on learning the
density discrimination. We note that they had these response
tendencies despite the lack of transparent feedback, but den-
sity-discrimination performance is presumably based on a
primary representation. The remaining question is: Do we
need to hypothesize a secondary representation to explain the
use of the uncertainty response? Because response strengths
for “S” and “D” are expected to decline toward the most dif-
cult density discriminations, a at low-frequency threshold
for the “?” would selectively produce higher response ten-
dencies for “?” at the difcult discriminations. By contrast,
as the density discrimination becomes easier for sparse and
dense problems, “S” and “D” response strengths would pro-
gressively begin to exceed the response strength for “?”. In
addition to the history of reinforcement of the joystick re-
sponse described above, there also may have been a residual
source of concurrent reinforcement that would maintain the
tendency to select “?” at a relatively low frequency. The
selection of the uncertainty response would reduce delay to
reinforcement in the next block of trials as outlined in the
simulation above. Consequently, reinforcements per unit
time would be higher when the monkey selected the uncer-
tain option (which would be primarily restricted to difcult
discriminations based on a comparison of response strengths
as outlined above) compared to the scenario of not using the
uncertain option. It is worth noting that the above analysis
does not require that we assume uncertainty monitoring of a
secondary representation. All that is required is a compari-
son of response strength of “?” (which is relatively low and
at) with the response strength of “S” and “D”, which de-
cline for difcult discriminations. Previous reinforcement of
the joystick is sufcient to produce a constant attractiveness
of this option. Moreover, the level of the low threshold for
the uncertainty response could be maintained by sensitivity
to food per unit time as suggested by the simulation above.
Therefore, the analysis from Figure 3 may apply even to this
study.
It is worth noting that although this is an impressive pro-
cedure that made signicant progress in making feedback on
the primary task opaque, these features of the experiment do
not eliminate response strengths for the primary task. The
monkeys in Smith and colleagues’ (2006) study responded
with higher accuracy on easy problems near the end of the
stimulus continuum compared to difcult problems near the
middle of the stimulus continuum. Thus, we could trace out
a psychophysical function for the sparse-dense continuum.
Metacognition in Animals 11
This function is consistent with high response tendencies
to respond “sparse” for the least-dense stimuli and to re-
spond “dense” for the most-dense stimuli. Thus, response
strengths appear to be much like what would be observed
if feedback was transparent. To claim otherwise amounts
to claiming that the animals do not have a customary psy-
chophysical function. The above discussion suggests that
it is reasonable to assume that the animals have response
strengths for the primary task that appear to be similar to
the response strength functions used in Smith et al.’s (2008)
model. Although it is quite impressive that the animals learn
the sparse-dense discrimination despite delayed and re-or-
dered feedback, once such learning has been documented,
we can infer the existence of response strength tendencies
and apply Smith et al.’s (2008) model.
It is also worth noting that asymmetries in the primary
task and in the use of the uncertainty response do not provide
denitive evidence for metacognition. In particular, Smith et
al.’s (2006) monkey had a leftward shift in its use of sparse,
dense, and uncertainty responses. If there is no response
bias, then a subject would be expected to have response ten-
dencies that are symmetrically distributed across the sparse-
dense continuum. For example, in a discrimination with 41
stimulus levels, the frequency of sparse and dense responses
would be expected to cross over at the middle stimulus level
(i.e., 21) assuming a linear scale. Instead, the cross-over
point occurred at approximately stimulus 16. The highest
response proportion also occurred for stimulus level 16,
but the distribution of all uncertain responses appears to be
shifted even further to the left. Smith et al. (2008) argue that
the leftward shift in the uncertainty-response distribution
provides strong evidence for uncertainty monitoring. We of-
fer an alternative explanation. The monkey had a relatively
strong bias to judge displays as dense; the monkey was virtu-
ally perfect on all dense displays. Accuracy variation across
stimuli was mainly restricted to the sparse response, with vir-
tually perfect performance at the eight sparsest stimulus lev-
els. If a psychophysical function plotted the probability of a
sparse response as a function of stimulus level, the function
would be shifted toward the left (i.e., the point of subjective
equality [p(sparse response)=.5] was below stimulus level
21). The standard way to model this type of data pattern in a
primary sparse-dense task is to propose that the psychophys-
ical function for density is biased toward the left (Blough,
1998, 2000). Similarly, the uncertainty response is biased to
the left, although the magnitude of the bias is slightly large
in the case of the uncertainty response. A bias parameter is
needed for both distributions, and the only anomaly is that
the bias is slightly larger in one of the cases. From another
perspective, it is worth noting that a low-level model pre-
dicts the use of the uncertainty response for difcult stimuli
in the experiment reported by Smith et al. (2006), although
without an extra parameter, it cannot account for the exact
location of the peak. Although these small modications to
the generalization account increase its complexity, the use of
bias parameters to explain a small difference in an individu-
al subject’s data is not unprecedented. Moreover, a slightly
more complex generalization model would remain less com-
plex than the proposal that animals exhibit metacognition.
Summary. Despite creative attempts to curtail reinforce-
ment, the functional use of an uncertainty response may be
due to the existence of residual reward variables. Indeed, if
an uncertainty response was never reinforced, it seems un-
likely that it would be produced by the subject, and it seems
more unlikely that it would be used functionally to express
uncertainty or escape a difcult trial
4
. We note that this pes-
simistic assessment is not meant to restrict inquiry. Instead,
it is our hope that recognizing the limits of existing methods
may help foster the development of new methods to assess
the use of a secondary representation.
Transfer Tests
Given the pervasiveness of reinforcement variables in the
training of decline or uncertainty responses, despite careful
attempts to curtail reinforcement, it is important to examine
alternative techniques that do not try to eliminate reward.
The transfer test is the major technique that is used to test
a stimulus-response hypothesis. In a transfer test, stimuli
from training are replaced with new stimuli in test. Although
there is an intuitive appeal to the transfer test methodology,
the formal situation in a transfer test is much the same as
discussed above. Thus, the animal’s uncertainty behavior
in a new stimulus context may be explained by low-level
mechanisms (as outlined below).
Formal modeling of transfer test methodology. If uncer-
tainty responding is conditioned on occurrence of a specic
stimulus, then transferring to a novel stimulus context is
sufcient to prevent application of the stimulus-response
mechanism. Thus, it is intuitive that the functional use of
the uncertainty response in a novel stimulus context would
strengthen the claim that generalized uncertainty rather
than stimulus context controls uncertainty responding
(i.e., metacognition). Although a transfer test is a powerful
technique to assess representations that govern performance
in many domains (Cook & Wasserman, 2007; Heyes, 1993;
Reid & Spetch, 1998; Wright & Katz, 2007), an analysis of
low-level mechanisms suggests that this intuition does not
apply in the case of metacognition (details to support this
conclusion appear below).
Typically, experiments with monkeys use relatively task-
savvy subjects with a long history of participating in labora-
tory tasks. Thus, these subjects bring to each new experiment
Metacognition in Animals 12
an extensive repertoire of experiment-related behaviors. In-
deed, the ability to readily draw on this behavioral repertoire
facilitates using such experienced subjects. For example, the
monkeys have extensive experience with joysticks and mov-
ing a cursor to target locations. Consequently, these sub-
jects may generalize from earlier experiments to the current
experiment. As described above, this generalization is not
surprising given the similarity between earlier experiments
and a current experiment (e.g., the monkeys approached the
perch to view the video display, reached through the cage
mesh to manipulate the joystick below the monitor, moved
the joystick so that the cursor on the screen contacted com-
puter-generated stimuli, etc.); all of these factors promote
the use of responses from their experimental repertoire in
new experiments, thereby allowing the experimenters to for-
go the extensive training that would otherwise be required if
new subjects were tested in each experiment.
In our analysis of transfer tests, uncertainty responding
is modeled by a at, low-frequency threshold in a transfer
test because the uncertainty response is stimulus indepen-
dent. In each case, response strengths determine selection
of the uncertainty or transfer response. It is worth noting
that a stimulus independent mechanism can operate in paral-
lel with a stimulus-response mechanism. Consider the situ-
ation in which an animal learned a stimulus-response rule
for a set of specically trained stimuli. In a transfer test,
the previously trained stimuli are not presented, and so the
stimulus-response function is not available to guide the use
of a decline response. However, if the animal also has a
low-frequency tendency to select the response in a stimu-
lus independent fashion, then what remains in the transfer
condition is the low-frequency threshold. In such a situa-
tion, a generalization decrement would be expected for the
stimulus-response mechanism but not for the stimulus-inde-
pendent mechanism. In any case, a low-frequency tendency
to select a decline response may exist once it has a history
of reinforcement. Our goal is to evaluate the ability of this
simple mechanism when the animal is subjected to a transfer
test. We consider three types of transfer tests.
Case 1: Training on the primary task withholds a subset
of stimulus conditions to be used for a future transfer test.
Figure 6 shows the formal situation using a memory task at
multiple retention intervals. The animal has been trained on
the primary task using a variety of stimulus conditions (i.e.,
retention intervals), but a subset of stimulus conditions have
been withheld (i.e., these stimuli have been reserved for use
in a future test). When the retention interval is unusually
short, trace strength is unusually high (and higher than the
uncertainty response). For longer retention intervals, it is
increasingly likely that the uncertainty option will be select-
ed. As discussed above (see section on metamemory), the
memory trace decay continuum is a primary representation
absent specic data that would pinpoint the use of a second-
ary representation. Note that a graded level of transfer is
expected in Case 1 (with more responding to transfer test A
than to transfer test B, which is higher than transfer test C).
Case 2: Training has occurred on two primary tasks, but
the uncertainty response has not been presented in the trans-
fer task prior to collection of the critical transfer data. Fig-
ure 7 shows the formal situation using two two-alternative
forced choice tasks. Training on one discrimination (i.e.,
stimulus dimension 1, responses 1 and 2 in the gure) in-
cluded the uncertainty response, whereas training on the
other discrimination (i.e., stimulus dimension 2, responses
3 and 4) did not include the uncertainty option; the presen-
tation of the uncertainty option together with stimulus di-
mension 2 has been reserved for use in a future transfer test.
When the transfer task is difcult, the uncertainty response
has the highest response strength. When the uncertainty op-
tion is presented with the transfer task for the rst time, the
response strength gradients are available for the transfer task
based on previous training. Note that Responses 3 and 4 are
expected to occur at the extreme ends of stimulus dimen-
sion 2 in the transfer test in Case 2, whereas the uncertainty
response is expected to occur for intermediate stimuli based
on the primary representations.
Case 3: Training has occurred with a primary task and
the uncertainty response, and transfer assesses an untrained
task. Thus, the uncertainty response and the primary task,
but not the transfer task, are well trained. Figure 8 shows the
Memory Trace Decay
Memory response
Uncertainty response
Transfer test A
Transfer test B
Transfer test C
Retention Interval
Response Strength
Figure 6. Schematic of response-strength model for a
memory task using transfer to novel retention intervals.
The primary task is well trained, and use of the uncer-
tainty response has occurred along the trained stimulus
continuum. Square, circle, and diamond represent re-
sponse strengths for novel stimuli (i.e., novel retention
intervals).
Metacognition in Animals 13
Stimulus dimension 1 Stimulus dimension 2
Primary Response 1
Primary Response 2
Uncertainty
Primary Response 3
Primary Response 4
Uncertainty
Primary Secondary
Response Strength
Figure 7. Schematic of response-strength model for two well-trained two-alternative forced-choice procedures. When the
uncertainty option is presented with the transfer task for the rst time, the response strength gradients are available for the
transfer task (based on previous training).
formal situation. Unlike Case 2 above, training has occurred
only on stimulus dimension 1. Thus, response-strength gra-
dients are absent in the transfer test because the transfer task
is not yet trained. This is the most difcult transfer case to
model because assumptions need to be made about the re-
sponse strengths in the untrained primary task. We assume
that response strengths would be low for the untrained, pri-
mary-task response options, in which case the uncertainty
option likely has the highest response strength, on average;
the same situation occurs when a to-be-remembered item is
omitted as a transfer test. Note that in Case 3, the uncer-
tainty response is expected to win compared to the untrained
task (transfer stimuli A, B, and C).
The analysis of the three cases above focused on evaluating
the implications of a at low-frequency threshold for the un-
certainty response. However, the above analysis also applies
to the case of a stimulus-response hypothesis in the follow-
ing way. Suppose that an animal learns a specic stimulus-
response rule. To be concrete, let’s consider Case 2 above, in
Uncertainty
Transfer A
Transfer B
Transfer C
Primary Response 1
Primary Response 2
Uncertainty
Stimulus dimension 1 Stimulus dimension 2
Primary Transfer
Response Strength
Figure 8. Schematic of response-strength model for one well-trained two-alternative forced-choice procedure. Training
has occurred with a primary task and the uncertainty response (together), and transfer assesses an untrained task. Re-
sponse-strength gradients are absent in the transfer test because the transfer task is not yet trained. Square, circle, and
diamond represent response strengths for novel stimuli.
Metacognition in Animals 14
which the decline response is trained on stimulus dimension
1 and examined in a transfer test using stimulus dimension 2.
If the animals have learned a stimulus-response rule in Case
2, then an inverted U-shaped function would appear in the
left panel of Figure 7 (in place of the at response threshold
in the left panel of Figure 7). A transfer test is well suited to
test this stimulus-response hypothesis because the transfer
test uses stimuli from stimulus dimension 2, in which case
none of the stimuli in the original stimulus-response rule are
available in the transfer test. This is the conventional ratio-
nale for a transfer test. However, we need to evaluate the
implications of an ineffective stimulus-response rule in the
transfer condition. What is the attractiveness of the decline
response in the transfer test (i.e., in stimulus dimension 2)?
Because a stimulus-response rule has not been learned for
any of the stimuli in dimension 2, the stimuli in dimension
2 would support only a very low-level of attractiveness, and
this attractiveness would be constant across stimuli in di-
mension 2. Thus, the next step in our analysis is to evaluate
the predictions of a low-frequency threshold for the uncer-
tainty response. Of course, this is what is displayed in the
right panel of Figure 7, and Smith et al.’s (2008) model can
predict apparently functional use of the uncertainty response
and a performance difference based on a winner-take all rule
applied to response strengths. Thus, we conclude that the
status of stimulus-response learning in the original task is
not critical to our analysis of the transfer test.
In each case, putative transfer of metacognition can be
based on low-level, response-strength mechanisms. Al-
though transfer tests are a powerful technique to evaluate
stimulus-response hypotheses, they are of limited utility
here because the low-level mechanism may be stimulus in-
dependent (i.e., a low-frequency, at threshold).
Parsimony and metacognition
We have argued that explanations based on primary rep-
resentations should be tentatively accepted before asserting
explanations based on secondary representations. In this re-
spect, Smith et al.’s (2008) response-strength model is less
complex than a metacognition model. In our review, we
found that the existing data on uncertainty responses can be
explained by a low-level model without appealing to meta-
cognition. It is important to note that the situation would
change dramatically if other data were to emerge that could
not be explained by low-level models but could be explained
by metacognition. In that situation, we would agree that ani-
mals are capable of metacognition. Moreover, if new data
emerged that required a metacognitive explanation, then we
would encourage a re-evaluation of older data. If animals
were shown to be metacognitive in some tasks, then it would
not be simpler to invoke alternative explanations for the re-
maining cases. For example, consider a case in which puta-
tive metacognition tasks 1-5 were adequately explained by
low-level mechanisms but new tasks 6-7 emerged that could
only be explained by metacognition. In this case, we would
support the reinterpretation of all of the data as metacogni-
tion given the converging lines of evidence. Thus, there is
a great need to explore new methods that can be explained
by metacognition but cannot be explained by a low-level hy-
pothesis.
Conclusions
We believe that existing methods have approached the dif-
cult problem of metacognition in innovative and creative
ways. A large array of techniques are being used (examina-
tion of accuracy predications, attempts to curtail reinforce-
ment of uncertainty responses, uncoupling of feedback from
the responses that earned the feedback). Although our as-
sessment is that existing methods do not pinpoint the use
of a secondary representation, we are optimistic that new
methods can be developed. The objective of developing
new methods would be to make predictions that cannot be
explained based on primary representations alone.
Smith and colleagues’ (2008) use of a at threshold in
their models has far-reaching implications. It suggests that
stimulus-response learning about an uncertainty response
(i.e., a curved or inverted U-shaped function) is not required
for apparently functional use of the uncertainty response.
Moreover, an independent line of evidence from accuracy
data (i.e., a Chosen-Forced performance advantage) is not
available from established methods. In addition, it is de-
sirable to simulate low-level mechanisms before conduct-
ing new experiments. The advantage of such an approach is
that it requires precise specications of the method and the
model. Such an approach may be helpful in identifying new,
innovative methods that can pinpoint the use of a secondary
representation (i.e., a method in which some pattern of data
is not predicted by application of a primary representation
alone).
We believe that an assessment of what is ‘lost’ in terms
of existing metacognition methods and data may prompt the
development of new methods to examine metacognition that
are not susceptible to low-level explanations. Such an as-
sessment is critical for the development of new standards
by which to evaluate tests of metacognition. A periodic re-
evaluation of standards will facilitate progress in our under-
standing of metacognition in animals.
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Footnotes
1
We note that Carruthers’s rst-order explanation proposes
that a “gate-keeping” mechanism is used to select from
differing goals, each with a different degree of strength,
thereby determining a behavioral outcome. In our analysis
that follows, it is not necessary to propose a gate-keeping
mechanism. Rather a winner-take all response rule is used
to select a response with the highest response strength.
2
Smith et al. (2008) described two alternative proposals and
Staddon and colleagues (Jozefowiez, Staddon, & Cerutti,
submitted; Staddon, Jozefowiez, & Cerutti, 2007) have
described an additional alternative. Each proposal has
a similar function form for the decision-making process.
Thus, we examine in detail one of Smith et al.’s proposals
here.
3
We used 0.7 for the “sens” parameter in Smith et al.
(2008), and for variability in mapping physical stimuli into
subjective representations, we used a normal distribution
with a mean of 0 and a standard deviation of 1.5. The
delays to reinforcement were based on information from
Beran et al. 2006 (20-s time out for incorrect responses, 1-
s inter-trial interval), and we estimated the amount of time
for viewing the stimuli and producing the choice response
at 2 s. The center value for the primary discrimination
was 5.
4
A subject may engage in observing responses to test the
functional role played by different response options.
Although observing responses may have a basis in
reinforcement (De Lorge & Clark, 1971; Shahan &
Podlesnik, 2008; Steiner, 1970; Zentall, Clement, &
Kaiser, 1998; Zentall, Hogan, Howard, & Moore, 1978),
even if they did not have a basis in reinforcement, the
Smith et al. (2008) low-level model could be applied to
this situation because observing responses may occur in a
stimulus independent fashion.
... My reaction (after simulating the model and observing the same pattern as in our data) was to change my view. I no longer believe that rats demonstrate metacognition (Crystal, 2012(Crystal, , 2014(Crystal, , 2019Crystal & Foote, 2009a, 2009b. A number of simple models also suggest that monkeys and rats do not demonstrate metacognition (Crystal & Foote, 2009a;Jozefowiez et al., 2009;Le Pelley, 2012. ...
... I no longer believe that rats demonstrate metacognition (Crystal, 2012(Crystal, , 2014(Crystal, , 2019Crystal & Foote, 2009a, 2009b. A number of simple models also suggest that monkeys and rats do not demonstrate metacognition (Crystal & Foote, 2009a;Jozefowiez et al., 2009;Le Pelley, 2012. Perhaps the headline that rats demonstrate metacognition was a misdirection, but in this instance it changed what we think about metacognition in nonhuman primates. ...
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... Various explanations that do not require metacognition have been proposed for this information-seeking behavior. In experiments involving escape response paradigms, it has been noted that monkeys might rely on external cues to monitor their behavior without truly being aware of their knowledge state (Crystal and Foote 2009;Jozefowiez et al. 2009;Smith et al. 2009). Although the tube task requires much less training, it is still possible that subjects learn, during testing, to associate observable cues with outcomes, such as looking inside the tubes. ...
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Chapter
The chapter describes the link between episodic memory and autonoetic consciousness. Autonoetic conscious is needed to allow a person to travel mentally through his own personal past, free of the immediate stimulus environment. The chapter delineates the relationship between this kind of episodic memory and the ability to project into the future. As per this chapter, the latter is the kernel of consciousness that is necessary for culture. It also suggests a practical test called the "spoon test," as a method of determining, without language, whether a person or an animal possesses autonoetic consciousness. One long-lasting virtual tug-of-war has to do with the nature of the similarities and differences between species. The chapter argues that only human beings possess "autonoetic" episodic memory and the ability to mentally travel into the past and into the future.
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Forgetting functions describe how accuracy or discriminability declines as the temporal distance from the event to be remembered increases. Several two-parameter mathematical functions are equally successful in fitting data from a range of studies. The choice of function must therefore be made on theoretical grounds. Consistent with the proposal that remembering follows the principles of discrimination, remembering is specific to the time of retrieval and is independent of the level of performance at earlier times in the retention interval. Empirical evidence for this temporal independence supports constant-rate forgetting. Exponential functions are therefore favored descriptions of forgetting functions because they describe how the influence of the temporally distant event declines at a constant rate. A combination of exponential generalization with an exponential decrease in the effect of the temporally distant stimulus holds promise as a theoretical account of forgetting functions.
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Three methods (anecdote collection, conditional discrimination training and trapping) used to investigate the possibility that primates attribute mental states are evaluated with reference to recent studies employing these methods. No convincing evidence of the phenomenon is found, and it is argued that none of these current methods could provide such evidence. In each case, behaviour consistent with the attribution of a mental state to an interactant could also be the result of associative or inferential learning about observable properties of the interactant's appearance or behaviour. A fourth method of investigation, which triangulates on mental state attribution using conditional discrimination training followed by transfer tests, is recommended as having the potential to provide evidence of mental state attribution in animals. It is argued that progress in this field has been hampered by a lack of full recognition that animals may learn inferentially about observables, and engage in associative learning without explicit training; and by misconstrual of the relationship between 'behaviourism' and mental state attribution.
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Observing behavior of two squirrel monkeys was examined under a multiple schedule of four components. Lever (observing) responses produced either a stimulus indicating the availability of food or another stimulus indicating food was not available. Key responses in the presence of the food-available stimulus produced food on a continuous reinforcement schedule. In the absence of food-available stimuli, responding on the key had no scheduled consequences. Observing responses produced food-available stimuli according to three different random-interval schedules with mean interstimulus availability times of 1, 2, and 4 min. In the fourth component of the multiple schedule (observing extinction) food-available stimuli never occurred. Each component of the schedule was correlated with a distinctive auditory stimulus. Observing rates decreased with decreasing frequency of the food-available stimulus. Observing rates during extinction continued decreasing when the brief stimulus indicating food unavailability was no longer produced by lever pressing. When the brief stimulus was reinstated response rates increased abruptly.
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The observing response paradigm was used to assess the reinforcing properties of discriminative stimuli by allowing animals either to work for food in the presence of a neutral stimulus or to first make an observing response by pressing a lever. On a progressive ratio schedule this resulted in the appearance of easily discriminable stimuli which marked positive and negative trials. The uncertainty associated with the imposed neutral stimulus was varied by manipulating the proportion of positive and negative trials in the session. The animals switched most often when the probability of reinforcement was low, less often when it was intermediate, and least often when it was high. This was not consistent with an uncertainty reduction hypothesis but could be explained if the uncertainty had to do with response rather than outcome.
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In a psychophysical approach to remembering, the events to be remembered are discriminated from other possibilities at the time of remembering, and not at the time of encoding or learning. The discrimination is specific to the retention interval at which remembering occurs, as shown by experiments demonstrating that discriminability and response bias are delay–specific. This article discusses a discrimination model for remembering that emphasizes the individual's history of learning about reward payoffs in similar experiences in the past. This model predicts the two characteristics of forgetting functions, initial discriminability and rate of forgetting.