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Uncertain responses by humans and Rhesus monkeys (Macaca mulatta) in a psychophysical same–different task.
Abstract
The authors asked whether animals, like humans, use an uncertain response adaptively to escape indeterminate stimulus relations. Humans and monkeys were placed in a same-different task, known to be challenging for animals. Its difficulty was increased further by reducing the size of the stimulus differences, thereby making many same and different trials difficult to tell apart. Monkeys do escape selectively from these threshold trials, even while coping with 7 absolute stimulus levels concurrently. Monkeys even adjust their response strategies on short time scales according to the local task conditions. Signal-detection and optimality analyses confirm the similarity of humans' and animals' performances. Whereas associative interpretations account poorly for these results, an intuitive uncertainty construct does so easily. The authors discuss the cognitive processes that allow uncertainty's adaptive use and recommend further comparative studies of metacognition.
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“The task design, a form of post-decision wagering (26–28), ensured that the monkey made a decision about motion direction on each trial.”
From Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex (2009) · cites this paper as [27]
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Shadlen, M. N., & Kiani, R. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.047 · Cited by 694
“However, introduction of postdecision wagering has begun to change this (Hampton, 2001; Kepecs et al., 2008; Kiani and Shadlen, 2009; Kornell et al., 2007; Middlebrooks and Sommer, 2012; Shields et al., 1997).”
BackgroundHow we know our own minds: The relationship between mindreading and metacognition
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Transfer of metacognitive skills and hint seeking in monkeys
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A computational framework for the study of confidence in humans and animals
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“Note that the same critique applies to the similar studies of monkeys performing psychophysical pixel density tasks ( Shields, et al., 1997 ).”
ResultThe study of animal metacognition
Smith, J. D. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.06.009 · Cited by 203
Self-citationTowards a comparative science of emotion: Affect and consciousness in humans and animals
Paul, E. S., Sher, S., Tamietto, M., Winkielman, P., & Mendl, M. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.014 · Cited by 180
“Using a range of methodologies, evidence has built for metacognitive capacities across a range of species, including chimpanzees and orangutans (Call and Carpenter, 2001), rhesus macaques (Macacca mulatta, Shields et al., 1997; Hampton, 2001) and rats (Kepecs et al., 2008).”
BackgroundInformation seeking by rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella)
Beran, M. J., & Smith, J. D. (2011) · Cognition · doi:10.1016/j.cognition.2011.02.016 · Cited by 161
Self-citationThe comparative study of metacognition: Sharper paradigms, safer inferences
Smith, J. D., Beran, M. J., Couchman, J. J., & Coutinho, M. V. C. (2008) · Psychonomic Bulletin & Review · doi:10.3758/pbr.15.4.679 · Cited by 151
Self-citationSmith, J. D., Beran, M. J., Redford, J. S., & Washburn, D. A. (2006) · Journal of Experimental Psychology General · doi:10.1037/0096-3445.135.2.282 · Cited by 142
Self-citationGrimaldi, P., Lau, H. C., & Basso, M. A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.006 · Cited by 138
“…into the nature of confidence, one limitation is that they used relatively simple quantitative analysis, such as how often an ambiguous stimulus was followed by a sure choice (Shields et al., 1997) or how often a correct choice was endorsed with a high confidence judgment (Son and Kornell, 2005).”
BackgroundResultInfluentialMetacognition in animals: how do we know that they know?
Jozefowiez, J., Staddon, J. E. R., & Cerutti, D. T. (2009) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2009.40003 · Cited by 125
“Indeed, in dolphins (with tones Smith et al., 1995), rhesus monkeys (with both stimuli differing in terms of pixel density , Shields et al., 1997), or number of elements (Washburn et al., 2006), rats (with stimuli differing in terms of their duration, Foote & Crystal, 2007) and pigeons (with…”
BackgroundAn assessment of memory awareness in tufted capuchin monkeys (Cebus apella)
Basile, B. M., Hampton, R. R., Suomi, S. J., & Murray, E. A. (2008) · Animal Cognition · doi:10.1007/s10071-008-0180-1 · Cited by 123
“1995) and rhesus monkeys show the same pattern for visual discriminations (Shields et al. 1997; Smith et al. 2006; Smith et al. 1997).”
Spontaneous Metacognition in Rhesus Monkeys
Rosati, A. G., & Santos, L. R. (2016) · Psychological Science · doi:10.1177/0956797616653737 · Cited by 115
Information seeking by orangutans: a generalized search strategy?
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“As a starting point, Smith and colleagues pioneered research on so-called ‘uncertainty monitoring’ in several species, including rats, bottlenosed dolphins, monkeys, and humans (Shields et al. 1997; Smith and Schull 1989; Smith et al. 1995, 1997).”
BackgroundDo orangutans (Pongo pygmaeus) know when they do not remember?
Suda-King, C. (2007) · Animal Cognition · doi:10.1007/s10071-007-0082-7 · Cited by 101
Category Learning in Rhesus Monkeys: A Study of the Shepard, Hovland, and Jenkins (1961) Tasks.
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“Whereas our monkeys have sometimes shown symbolic or relational learning and sophisticated cognitive accomplishments (Shields et al., 1997; Smith et al., 1998, 2003a; Washburn, 1994; Washburn & Rumbaugh, 1991a), they have also sometimes shown equally dramatic failures of cognitive performance (Filion, 1993; Washburn,…”
BackgroundSelf-citationRhesus macaques (macaca mulatta) monitor uncertainty during numerosity judgments.
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Self-citationInformation seeking in capuchins (Cebus apella): A rudimentary form of metacognition?
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“This research and other initial reports on metamemory suggested that dolphins and rhesus macaques metacognitively monitor their uncertainty (Beran et al. 2006; Hampton 2001; Shields et al. 1997; Smith et al. 1996, 1998), whereas capuchin monkeys (Cebus apella; a New World monkey species), pigeons (Columba livia), and…”
BackgroundCrystal, J. D., & Foote, A. L. (2009) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2009.40001 · Cited by 86
The highs and lows of theoretical interpretation in animal-metacognition research
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Self-citationSuperior colliculus neuronal ensemble activity signals optimal rather than subjective confidence
Odegaard, B., Grimaldi, P., Cho, S. H., Peters, M. A. K., Lau, H. C., & Basso, M. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1711628115 · Cited by 78
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“Addressing this possibility, we (Shields et al., 1997) asked whether monkeys could make adaptive uncertainty responses when pushed to their perceptual limit in a same/different task.”
BackgroundSelf-citationSome task demands induce collapsing bounds: Evidence from a behavioral analysis
Palestro, J. J., Weichart, E. R., Sederberg, P. B., & Turner, B. M. (2018) · Psychonomic Bulletin & Review · doi:10.3758/s13423-018-1479-9 · Cited by 77
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“In some trials, the chimpanzees demonstrated behavior consistent with uncertainty or lack of confidence about their choices [Shields et al., 1997].”
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“1995), monkeys, and humans (Shields et al. 1997) made one of two judgments about a psychophysical stimulus (e.”
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“Rhesus monkeys, bottlenose dolphins, and humans show metacognitive responding by successfully declining difficult visual or auditory discrimination tests (e.g. recognizing auditory stimulus as high- and low-pitched; Shields et al. 1997) when the stimuli were near the discriminatory threshold.”
BackgroundBeran, M. J., Perdue, B. M., Futch, S. E., Smith, J. D., Evans, T. A., & Parrish, A. E. (2015) · Cognition · doi:10.1016/j.cognition.2015.05.023 · Cited by 66
Self-citationRetrospective and prospective metacognitive judgments in rhesus macaques (Macaca mulatta)
Morgan, G., Kornell, N., Kornblum, T., & Terrace, H. S. (2013) · Animal Cognition · doi:10.1007/s10071-013-0657-4 · Cited by 55
“The earliest research on metacognitive monitoring in animals used psychophysical paradigms to compare the use of an “uncertain” response by humans, monkeys, and a dolphin (Shields et al. 1997; Smith et al. 1995).”
Uncertainty promotes information-seeking actions, but what information?
Keller, A. M., Taylor, H. A., & Brunyé, T. T. (2020) · Cognitive Research Principles and Implications · doi:10.1186/s41235-020-00245-2 · Cited by 69
The interplay between uncertainty monitoring and working memory: Can metacognition become automatic?
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Self-citationSole, L. M., Shettleworth, S. J., & Bennett, P. (2003) · Psychonomic Bulletin & Review · doi:10.3758/bf03196540 · Cited by 45
“Like us, Smith and his colleagues (Shields et al., 1997; Smith et al., 1995; Smith et al., 1997) compared the behavior of their subjects with optimal behavior derived from signal detection theory.”
BackgroundNeindre, P. L., Bernard, É., Boissy, A., Boivin, X., Calandreau, L., Delon, N., Deputte, B. L., Desmoulin‐Canselier, S., Dunier, M., Faivre, N., et al. (2017) · EFSA Supporting Publications · doi:10.2903/sp.efsa.2017.en-1196 · Cited by 56
Suda, C., & Call, J. (2005) · Cognition · doi:10.1016/j.cognition.2005.01.005 · Cited by 37
“…study complements other recent studies that have used explicit measures of metacognition such as escaping in difficult trials (Hampton, 2001; Shields et al., 1997; Smith et al., 1995, 1998, 1997) or seeking additional information upon encountering incomplete data to solve a task (Call,…”
Information Seeking in Animals: Metacognition?
Roberts, W., McMillan, N., Musolino, E., & Cole, M. R. (2012) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2012.70005 · Cited by 39
“As an example of a psychophysical experiment, Shields, Smith, and Washburn (1997) trained rhesus monkeys to make same-different judgments between boxes containing pixel densities.”
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Zhu, B., Cruz-Garza, J. G., Yang, Q., Shoaran, M., & Kalantari, S. (2021) · Advanced Engineering Informatics · doi:10.1016/j.aei.2022.101718 · Cited by 34
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“Humans and animals produce nearly identical graphs in some uncertainty tasks (e.g., Shields et al., 1997).”
BackgroundSelf-citationMandell, D. J., & Sackett, G. P. (2008) · Developmental Psychobiology · doi:10.1002/dev.20251 · Cited by 30
Couchman, J. J. (2011) · Biology Letters · doi:10.1098/rsbl.2011.0536 · Cited by 30
Innis, A., Lane, S. D., Miller, E. R., et al. (1998) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1998.70-87 · Cited by 28
“, 1993), and an ‘‘uncertain’’ option in psychophysical judgments (Shields et al., 1997; Smith et al., 1995; Thomson, 1920).”
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Self-citationNot knowing what one knows: A Meaningful failure of metacognition in capuchin monkeys.
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“To address this, Shields et al. (1997) evaluated whether monkeys and humans would use the UR when engaging in a same/different relative discrimination task, where macaques did not classify a specific density level, but chose whether two pixel-density magnitudes were equivalent.”
BackgroundSelf-citationExplicit memory and cognition in monkeys
Hampton, R. R., Engelberg, J. W. M., & Brady, R. J. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2019.107326 · Cited by 18
Uncertainty Monitoring by Young Children in a Computerized Task
Beran, M. J., Decker, S. L., Schwartz, A. J., & Smith, J. D. (2012) · Scientifica · doi:10.6064/2012/692890 · Cited by 23
“To date, an uncertainty response has been included in tests of psychophysical discrimination in the visual, auditory, and temporal domains [19, 23, 24, 31], in tests of list memory, item memory, and spatial memory [21, 32, 33], in tests of two-choice discrimination learning [34], and in tasks involving judgments of qu…”
BackgroundSelf-citationA comparison of non-verbal and verbal indicators of young children’s metacognition
Roebers, C. M., Kälin, S., & Aeschlimann, E. A. (2019) · Metacognition and Learning · doi:10.1007/s11409-019-09217-4 · Cited by 18
A similar basis for judging confidence in monkeys and humans
Ferrigno, S., Bueno, G. L., & Cantlon, J. F. (2019) · Animal Behavior and Cognition · doi:10.26451/abc.06.04.12.2019 · Cited by 17
“The dolphin chose to skip hard trials, the ones near the numerous macaques, and humans have all been shown to pass these types of tasks (Beran et al., 2006; Lyons & Ghetti, 2011; Shields et al., 1997; Smith et al., 1995).”
BackgroundDon't look back on failure: spontaneous uncertainty monitoring in chimpanzees
Tomonaga, M., Kurosawa, Y., Kawaguchi, Y., & Takiyama, H. (2023) · Learning & Behavior · doi:10.3758/s13420-023-00581-5 · Cited by 16
“Depending on the task, an uncertainty response may cancel the current task or seek more information to solve the task (Call & Car-penter, 2001; Hampton, 2001; Shields et al., 1997; Smith et al., 1995).”
Sosnowski, M. J., & Brosnan, S. F. (2023) · Animal Cognition · doi:10.1007/s10071-023-01768-z · Cited by 24
Breaking the perceptual-conceptual barrier: Relational matching and working memory
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Self-citationFading perceptual resemblance: A path for rhesus macaques (Macaca mulatta) to conceptual matching?
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Self-citationChecking behavior in rhesus monkeys is related to anxiety and frontal activity
Bosc, M., Bioulac, B. H., Langbour, N., Nguyen, T. H., Goillandeau, M., Dehay, B., Burbaud, P., & Michelet, T. (2017) · Scientific Reports · doi:10.1038/srep45267 · Cited by 13
“The modulation of certainty has previously been reported in humans 15,33,34 and several animal species 4–6, 34, 35 .”
Monkey Metacognition Could Generate More Insight
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Macaque monkeys exhibit behavioral signs of metamemory in an oculomotor working memory task
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Couchman, J. J., Beran, M. J., Coutinho, M. V. C., Boomer, J. B., Zakrzewski, A. C., Church, B. A., & Smith, J. D. (2011) · British Journal of Developmental Psychology · doi:10.1111/j.2044-835x.2011.02065.x · Cited by 11
“Smith and colleagues (Shields et al., 1997; Smith et al., 1995; Smith et al., 1998; Smith et al. 1997; Smith et al., 2003) began this search by giving a dolphin and rhesus monkeys perceptual discrimination tasks that, in addition to primary task responses, included an opt-out response – often called the uncertainty re…”
BackgroundResultInfluentialSelf-citationThe Curious Incident of the Capuchins
Smith, J. D., Beran, M. J., Couchman, J. J., Coutinho, M. V. C., & Boomer, J. B. (2009) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2009.40008 · Cited by 12
“Finally, macaques respond uncertain adaptively when facing abstract memory and relational-judgment problems (Hampton, 2001; Kornell et all, 2005; Shields et al., 1997; Smith et al 1998).”
BackgroundSelf-citationStructure-Mapping Processes Enable Infants’ Learning Across Domains Including Language
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On the proposed role of metacognition in environment learning: recommendations for research
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“Further, effectively monitoring mnemonic cues, such as uncertainty, may promote metacognitive control processes (Shields et al., 1997), such as controlling learning (seeking more locational details) to avoid negative outcomes.”
BackgroundMetacognition in Nonhumans: Methodological and Theoretical Issues in Uncertainty Monitoring
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“2 (Top) The Same-Different discrimination task used by Shields et al. (1997). Monkeys had to determine whether two rectangles contained the same number of pixels or not.”
MethodInfluentialSelf-citationOptimal policy for uncertainty estimation concurrent with decision making
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Studying Metacognitive Processes at the Single Neuron Level
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Rosati, A. G., Felsche, E., Cole, M. F., Atencia, R., & Rukundo, J. (2024) · Cognition · doi:10.1016/j.cognition.2024.105898 · Cited by 6
“This work has found that several species will make opt-out responses (Castro & Wasserman, 2013; Foote & Crystal, 2012; Hampton, 2001; Kornell et al., 2007; Shields et al., 1997; Smith et al., 1995; Smith et al., 1997; Smith et al., 1998).”
BackgroundMissing Links in the Evolution of Language
Terrace, H. (2011) · Research and perspectives in neurosciences · doi:10.1007/978-3-642-18015-6_1 · Cited by 5
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Roberts, W., McMillan, N., Musolino, E., & Cole, M. (2012) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2012.7005 · Cited by 5
The Highs and Lows of Theoretical Interpretation in Animal-Metacognition Research
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Self-citationA dynamic model of deciding not to choosePreprint
Reynolds, A., Garton, R. F., Kvam, P. D., et al. (2019) · doi:10.31219/osf.io/zxp5u · Cited by 5
Navigating the Interface Between Learning and Cognition
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Self-citationAre monkeys sensitive to informativeness: An experimental study with baboons (Papio papio)
Reboul, A., Mascaro, O., Claidière, N., & Fagot, J. (2022) · PLoS ONE · doi:10.1371/journal.pone.0270502 · Cited by 3
Humans, animals and computers: Minding machines?
Wasserman, E. A. (2009) · Revista de psicología · doi:10.5354/0719-0581.2009.17119 · Cited by 2
“The earliest work with monkeys and humans was conducted by Shields, Smith, and Washburn (1997).”
BackgroundSmith, J. D., Church, B. A., Beran, M. J., & Washburn, D. A. (2018) · Springer eBooks · doi:10.1007/978-3-319-47829-6_1822-1 · Cited by 2
Self-citationThe comparative psychophysics of complex shape perception
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“For example, Shields et al. (1997) observed that rhesus macaques responded strongly and for hundreds of trials to the absolute cues in an SD task before Wnally achieving successful, two-item SD performance.”
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Arguing for a conscious emergence of language
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Stoll, F. M., & Procyk, E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/741561
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Li, X., Su, R., Chen, Y., & Yang, T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.14.464349
“This is consistent with many previous studies (Kiani & Shadlen, 2009; Komura et al., 2013; Shields et al., 1997; D. J. Smith, 2009), although they did not measure the reaction time of confidence or (un)certainty along.”
ResultInnovation and Problem-Solving
(2021) · Cambridge University Press eBooks · doi:10.1017/9781108564113.034
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Self-citationMetacognitive Monitoring and Control in Monkeys
Hampton, R. R. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108768450.026
(2022) · Cambridge University Press eBooks · doi:10.1017/9781108768450.019
Smith, J. D., Church, B. A., Jackson, B. N., et al. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1746
Self-citationBeran, M. J. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1530
Smith, J. D., Church, B. A., Beran, M. J., & Washburn, D. A. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1822
Self-citation(2020) · Society for Neuroscience eBooks · doi:10.1523/hon.011007
Language Models Do Not Possess the Uniquely Human Cognitive Ability of Relational AbstractionPreprint
Monk, B., Meyer, T., & Ngo, M. K. (2024) · Preprints.org · doi:10.20944/preprints202401.1681.v1
Language Models Do Not Possess the Uniquely Human Cognitive Ability of Relational AbstractionPreprint
Monk, B., Meyer, T., & Ngo, M. K. (2024) · Preprints.org · doi:10.20944/preprints202401.1681.v2
A non-verbal process dissociation procedure to disentangle explicit from implicit sequence learning
Malassis, R., Moscado, L., Sackur, J., & Németh, D. (2026) · Neuroscience of Consciousness · doi:10.1093/nc/niag021
“Even when no verbal report is obtained from participants, the evidentiary weight on conscious awareness is typically extrapolated from cases where verbal reports are available ( Shields et al. 1997; Goupil and Kouider 2016).”
Metadata
- Authors
- Shields, W. E., Smith, J. D., & Washburn, D. A.
- Affiliations
- University at Buffalo, State University of New York (US)
- Venue
- Journal of Experimental Psychology: General
- Published
- 1997
- Volume
- 126
- Issue
- 2
- Pages
- 147-164
- ISSN
- 0096-3445 (ISSN-L)
- 1939-2222
- OpenAlex
- W2073687691
- Cited by
- 142
- References
- 0
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 9 · 2021: 10 · 2020: 5 · 2019: 10 · 2018: 7 · 2017: 6 · 2016: 3 · 2015: 10 · 2014: 8 · 2013: 7 · 2012: 8
- FWCI
- 2.13
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Experimental Psychology General (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD06016, P01HD006016)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- uncertainty, metacognition, same-different task, rhesus monkeys, human-animal comparison, signal detection, response strategies, stimulus discrimination, associative learning, comparative cognition
- MeSH terms
- Adult, Animals, Attention, Discrimination Learning, Female, Humans, Macaca mulatta, Male, Problem Solving, Psychophysics, Sensory Thresholds, Species Specificity, Transfer, Psychology, Contrast Sensitivity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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