Comparison of human infants and rhesus monkeys on Piaget's AB task: evidence for dependence on dorsolateral prefrontal cortex
Abstract
This paper reports evidence linking dorsolateral prefrontal cortex with one of the cognitive abilities that emerge between 7.5-12 months in the human infant. The task used was Piaget's Stage IV Object Permanence Test, known as AB (pronounced "A not B"). The AB task was administered (a) to human infants who were followed longitudinally and (b) to intact and operated adult rhesus monkeys with bilateral prefrontal and parietal lesions. Human infants displayed a clear developmental progression in AB performance, i.e., the length of delay required to elicit the AB error pattern increased from 2-5 s at 7.5-9 months to over 10 s at 12 months of age. Monkeys with bilateral ablations of dorsolateral prefrontal cortex performed on the AB task as did human infants of 7.5-9 months; i.e., they showed the AB error pattern at delays of 2-5 s and chance performance at 10 s. Unoperated and parietally operated monkeys succeeded at delays of 2, 5, and 10 s; as did 12 month old human infants. AB bears a striking resemblance to Delayed Response, the classic test for dorsolateral prefrontal function in the rhesus monkey, and indeed performance on AB and Delayed Response in the same animals in the present study was fully comparable. These findings provide direct evidence that AB performance depends upon dorsolateral prefrontal cortex in rhesus monkeys and indicates that maturation of dorsolateral prefrontal cortex may underlie the developmental improvement in AB performance of human infants from 7.5-12 months of age. This improvement marks the development of the ability to hold a goal in mind in the absence of external cues, and to use that remembered goal to guide behavior despite the pull of previous reinforcement to act otherwise. This confers flexibility and freedom to choose and control what one does.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Executive function development, although protracted, emerges rapidly, as early as the first months of life.
“EF development, although protracted, emerges rapidly, as early as the first months of life (Diamond and Goldman-Rakic, 1989; Diamond, 2013, 2020).”
From Assessment of executive functions in school-aged children: A narrative review (2022) · cites this paper as Diamond and Goldman-Rakic, 1989
Primitive signs of inhibition and working memory can be observed in infancy.
“primitive signs of inhibition and working memory can be observed in infancy”
From Assessing Executive Function in Preschoolers (2012) · cites this paper as Diamond & Goldman-Rakic, 1989
Executive function emerges much earlier than early adolescence.
“It is now well established that executive function emerges much earlier than this”
From Assessing Executive Function in Preschoolers (2012) · cites this paper as Diamond & Goldman-Rakic, 1989
Cites
Mountcastle, V. B., Lynch, J. C., Georgopoulos, A., Sakata, H., & Acuna, C. (1975) · Journal of Neurophysiology · doi:10.1152/jn.1975.38.4.871 · Cited by 2,061 · cited 1× · see citing works
“Parietal cortex was selected as the site for the control lesion because (1) it has been implicated in spatial processing (Pohl 1973; Mountcastle et al. 1975; Ungerleider and Brody 1977; Brody and Pribram 1978) and some theories of AB performance give prominence to the spatial component of the task (Butterworth 1975; B…”
MethodArnsten, A. F. T., & Goldman-Rakic, P. S. (1985) · Science · doi:10.1126/science.2999977 · Cited by 549 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Holroyd, C. B., & Coles, M. G. H. (2002) · Psychological Review · doi:10.1037/0033-295x.109.4.679 · Cited by 4,027 · see citing works
Rice, D., & Barone, S. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108s3511 · Cited by 2,944 · see citing works
Executive function in preschoolers: A review using an integrative framework.
Garon, N., Bryson, S. E., & Smith, I. M. (2008) · Psychological Bulletin · doi:10.1037/0033-2909.134.1.31 · Cited by 2,695 · see citing works
Assessment and Development of Executive Function (EF) During Childhood
Anderson, P. (2002) · Child Neuropsychology · doi:10.1076/chin.8.2.71.8724 · Cited by 2,218 · see citing works
“Infants younger than 9 months of age have difficulty inhibiting previously learned responses, but by 12 months of age most infants can inhibit certain behaviors and shift to a new response set (Diamond, 1985; Diamond & Doar, 1989; Diamond & Goldman-Rakic, 1989).”
BackgroundMaturation of Cognitive Processes From Late Childhood to Adulthood
Luna, B., Garver, K. E., Urban, T. A., Lazar, N. A., & Sweeney, J. A. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00745.x · Cited by 1,351 · see citing works
A developmental functional MRI study of prefrontal activation during performance of a go-no-go task
Casey, B. J., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., Castellanos, F. X., Haxby, J. V., Noll, D. C., Cohen, J. D., et al. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.6.835 · Cited by 1,106 · see citing works
Functional brain development in humans
Johnson, M. H. (2001) · Nature Reviews Neuroscience · doi:10.1038/35081509 · Cited by 980 · see citing works
An adaptive coding model of neural function in prefrontal cortex
Duncan, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35097575 · Cited by 874 · see citing works
What has fMRI told us about the Development of Cognitive Control through Adolescence?
Luna, B., Padmanabhan, A., & O’Hearn, K. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.005 · Cited by 892 · see citing works
The Development of Executive Attention: Contributions to the Emergence of Self-Regulation
Rueda, M. R., Posner, M. I., & Rothbart, M. K. (2005) · Developmental Neuropsychology · doi:10.1207/s15326942dn2802_2 · Cited by 813 · see citing works
Executive Function in Typical and Atypical Development
Zelazo, P. D., & Müller, U. (2010) · The Wiley‐Blackwell Handbook of Childhood Cognitive Development · doi:10.1002/9781444325485.ch22 · Cited by 784 · see citing works
Verbal Working Memory Load Affects Regional Brain Activation as Measured by PET
Jonides, J., Schumacher, E. H., Smith, E. E., Lauber, E. J., Awh, E., Minoshima, S., & Koeppe, R. A. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.4.462 · Cited by 715 · see citing works
The development of nonverbal working memory and executive control processes in adolescents
Luciana, M., Conklin, H. M., Hooper, C. J., & Yarger, R. S. (2005) · Child Development · doi:10.1111/j.1467-8624.2005.00872.x · Cited by 567 · see citing works
Dias, R., Robbins, T. W., & Roberts, A. C. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-23-09285.1997 · Cited by 555 · see citing works
White matter development in adolescence: A DTI study
Asato, M. R., Terwilliger, R., Woo, J., & Luna, B. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp282 · Cited by 512 · see citing works
Age differences in affective decision making as indexed by performance on the Iowa gambling task
Cauffman, E., Shulman, E. P., Steinberg, L., Claus, E., Banich, M. T., Graham, S., & Woolard, J. (2010) · Developmental Psychology · doi:10.1037/a0016128 · Cited by 488 · see citing works
Knowing in the context of acting: the task dynamics of the A-not-B-error
Smith, L. B., Thelen, E., Titzer, R., & McLin, D. (1999) · Psychological Review · doi:10.1037/0033-295x.106.2.235 · Cited by 496 · see citing works
LUNA, B., & SWEENEY, J. A. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.035 · Cited by 467 · see citing works
The case of K.C.: contributions of a memory-impaired person to memory theory
Rosenbaum, R. S., Köhler, S., Schacter, D. L., Moscovitch, M., Westmacott, R., Black, S. E., Gao, F., & Tulving, E. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.10.007 · Cited by 433 · see citing works
Developmental Changes in Cognitive Control through Adolescence
Luna, B. (2009) · Advances in Child Development and Behavior · doi:10.1016/s0065-2407(09)03706-9 · Cited by 419 · see citing works
Gao, W., Alcauter, S., Elton, A., Hernandez-Castillo, C. R., Smith, J. K., Ramirez, J., & Lin, W. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu088 · Cited by 380 · see citing works
An interactive framework for examining prefrontal cognitive processes
Roberts, R. J., & Pennington, B. F. (1996) · Developmental Neuropsychology · doi:10.1080/87565649609540642 · Cited by 392 · see citing works
Executive functions in young children with autism
Griffith, E. M., Pennington, B. F., Wehner, E. A., & Rogers, S. J. (1999) · Child Development · doi:10.1111/1467-8624.00059 · Cited by 385 · see citing works
Genetic and neurochemical modulation of prefrontal cognitive functions in children
Diamond, A., Briand, L., Fossella, J., & Gehlbach, L. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.1.125 · Cited by 381 · see citing works
Self-citationToward a Neurodevelopmental Model of Obsessive–Compulsive Disorder
Rosenberg, D. R., & Keshavan, M. S. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00443-5 · Cited by 355 · see citing works
The dependence of span and delayed-response performance on prefrontal cortex.
D’Esposito, M., & Postle, B. R. (1999) · Neuropsychologia · doi:10.1016/s0028-3932(99)00021-4 · Cited by 350 · see citing works
Changes and challenges in 20 years of research into the development of executive functions
Hughes, C. (2011) · Infant and Child Development · doi:10.1002/icd.736 · Cited by 347 · see citing works
Anderson, V. A., Anderson, P., Northam, E., Jacobs, R., & Mikiewicz, O. (2002) · Child Neuropsychology · doi:10.1076/chin.8.4.231.13509 · Cited by 338 · see citing works
Regional Brain and Ventricular Volumes in Tourette Syndrome
Peterson, B. S., Staib, L., Scahill, L., Zhang, H., Anderson, C., Leckman, J. F., Cohen, D. J., Gore, J. C., Albert, J., & Webster, R. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.5.427 · Cited by 312 · see citing works
Hwang, K., Velanova, K., & Luna, B. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2825-10.2010 · Cited by 314 · see citing works
Language, social, and executive functions in high functioning Autism: a continuum of performance
Landa, R. J., & Goldberg, M. C. (2005) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-005-0001-1 · Cited by 296 · see citing works
Vriezen, E. R., & Pigott, S. E. (2002) · Child Neuropsychology · doi:10.1076/chin.8.4.296.13505 · Cited by 298 · see citing works
The Prefrontal Cortex: Functional Neural Development During Early Childhood
Tsujimoto, S. (2008) · The Neuroscientist · doi:10.1177/1073858408316002 · Cited by 291 · see citing works
Assessing Executive Function in Preschoolers
Anderson, P. J., & Reidy, N. (2012) · Neuropsychology Review · doi:10.1007/s11065-012-9220-3 · Cited by 293 · see citing works
Dawson, G., Munson, J., Estes, A., Osterling, J., McPartland, J., Toth, K., Carver, L., & Abbott, R. (2002) · Child Development · doi:10.1111/1467-8624.00411 · Cited by 281 · see citing works
Velanova, K., Wheeler, M. E., & Luna, B. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn012 · Cited by 277 · see citing works
Neurodevelopment and executive function in autism
O'Hearn, K., Asato, M., Ordaz, S., & Luna, B. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000527 · Cited by 274 · see citing works
Chapter 9 Neuronal development in human prefrontal cortex in prenatal and postnatal stages
Mrzljak, L., Uylings, H. B. M., Van Eden, G. G., & Judáš, M. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62681-3 · Cited by 247 · see citing works
Epidemiological and Laboratory Evidence of PCB-lnduced Neurotoxicity
Seegal, R. F. (1996) · Critical Reviews in Toxicology · doi:10.3109/10408449609037481 · Cited by 242 · see citing works
A neural marker of perceptual consciousness in infants
Kouider, S., Stahlhut, C., Gelskov, S. V., Barbosa, L. S., Dutat, M., de Gardelle, V., Christophe, A., Dehaene, S., & Dehaene-Lambertz, G. (2013) · Science · doi:10.1126/science.1232509 · Cited by 235 · see citing works
Lewis, E. E., Dozier, M., Ackerman, J., & Sepulveda-Kozakowski, S. (2007) · Developmental Psychology · doi:10.1037/0012-1649.43.6.1415 · Cited by 206 · see citing works
Child Development and Neuroscience.
Nelson, C. A., & Bloom, F. E. (1997) · Child Development · doi:10.1111/j.1467-8624.1997.tb01974.x · Cited by 236 · see citing works
Lambe, E. K., Krimer, L. S., & Goldman-Rakic, P. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08780.2000 · Cited by 204 · see citing works
Self-citationAbbruzzese, M., Ferri, S., & Scarone, S. (1997) · Neuropsychologia · doi:10.1016/s0028-3932(96)00095-4 · Cited by 192 · see citing works
Evans, D. W., Lewis, M. D., & Iobst, E. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00274-4 · Cited by 188 · see citing works
New Procedures to Assess Executive Functions in Preschool Children*
Espy, K. A., Kaufmann, P. M., Glisky, M. L., & McDiarmid, M. D. (2001) · The Clinical Neuropsychologist · doi:10.1076/clin.15.1.46.1908 · Cited by 162 · see citing works
Neuropsychological Correlates of Early Symptoms of Autism
Dawson, G., Meltzoff, A. N., Osterling, J., & Rinaldi, J. (1998) · Child Development · doi:10.2307/1132265 · Cited by 289 · see citing works
Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex
Woo, T.-U., Pucak, M. L., Kye, C. H., Matus, C. V., & Lewis, D. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00059-6 · Cited by 157 · see citing works
Nydén, A., Gillberg, C., Hjelmquist, E., & Heiman, M. (1999) · Autism · doi:10.1177/1362361399003003002 · Cited by 151 · see citing works
Outcome Measures for Clinical Trials in Down Syndrome
Esbensen, A. J., Hooper, S. R., Fidler, D., Hartley, S. L., Edgin, J., d'Ardhuy, X. L., Capone, G., Conners, F. A., Mervis, C. B., Abbeduto, L., et al. (2017) · American Journal on Intellectual and Developmental Disabilities · doi:10.1352/1944-7558-122.3.247 · Cited by 153 · see citing works
Ontogenesis of goal-directed behavior: anatomo-functional considerations
Kostović, I., Judaš, M., Petanjek, Z., & Šimić, G. (1995) · International Journal of Psychophysiology · doi:10.1016/0167-8760(94)00081-o · Cited by 139 · see citing works
Prefrontal Executive Function Syndromes in Children
Powell, K. B., & Voeller, K. K. S. (2004) · Journal of Child Neurology · doi:10.1177/08830738040190100801 · Cited by 137 · see citing works
Development of Working Memory Maintenance
Geier, C. F., Garver, K., Terwilliger, R., & Luna, B. (2009) · Journal of Neurophysiology · doi:10.1152/jn.90562.2008 · Cited by 136 · see citing works
van Eden, C. G., Kros, J. M., & Uylings, H. B. M. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)62680-1 · Cited by 135 · see citing works
Velanova, K., Wheeler, M. E., & Luna, B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1579-09.2009 · Cited by 129 · see citing works
Executive Function: Cognition and Behaviour in Adults with Autism Spectrum Disorders (ASD)
Johnston, K., Murray, K., Spain, D., Walker, I., & Russell, A. (2019) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-019-04133-7 · Cited by 113 · see citing works
The assessment of executive functioning in children
Henry, L. A., & Bettenay, C. (2010) · Child and Adolescent Mental Health · doi:10.1111/j.1475-3588.2010.00557.x · Cited by 75 · see citing works
Conejero, Á., Guerra, S., Abundis‐Gutiérrez, A., & Rueda, M. R. (2018) · Developmental Science · doi:10.1111/desc.12494 · Cited by 62 · see citing works
MUNSON, J., FAJA, S., MELTZOFF, A., ABBOTT, R., & DAWSON, G. (2008) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617708081393 · Cited by 65 · see citing works
Assessment of executive functions in school-aged children: A narrative review
Souissi, S., Chamari, K., & Bellaj, T. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.991699 · Cited by 56 · see citing works
Faja, S., Dawson, G., Sullivan, K., Meltzoff, A. N., Estes, A., & Bernier, R. (2016) · Autism Research · doi:10.1002/aur.1608 · Cited by 47 · see citing works
Calcyon upregulation in adolescence impairs response inhibition and working memory in adulthood
Vazdarjanova, A., Bunting, K., Muthusamy, N., & Bergson, C. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.14 · Cited by 20 · see citing works
Zebdi, R., Goyet, L., Pinabiaux, C., & Guellaï, B. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00195 · Cited by 13 · see citing works
- Authors
- Diamond, A., & Goldman-Rakic, P. S.
- Affiliations
- Yale University (US)
- ORCID
- Diamond, A.
- Venue
- Experimental Brain Research
- Published
- 1989
- Volume
- 74
- Issue
- 1
- Pages
- 24-40
- ISSN
- 0014-4819 (ISSN-L)
- 1432-1106
- OpenAlex
- W2165849169
- Cited by
- 628
- References
- 2
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 12 · 2023: 12 · 2022: 16 · 2021: 15 · 2020: 19 · 2019: 19 · 2018: 25 · 2017: 13 · 2016: 15 · 2015: 25 · 2014: 18 · 2013: 27 · 2012: 30
- FWCI
- 27.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Experimental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH-00298, MH-38456)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-10094)
- Topics
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
- Keywords
- A-not-B task, object permanence, dorsolateral prefrontal cortex, infant cognitive development, rhesus monkeys, prefrontal lesions, parietal lobe lesions, delayed response, goal-directed behavior, working memory
- MeSH terms
- Aging, Animals, Cognition, Female, Frontal Lobe, Humans, Infant, Longitudinal Studies, Macaca, Macaca mulatta, Male, Reaction Time, Sex Factors
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.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
