Cited by 1,068Neural and Behavioral Psychology StudiesVisual perception and processing mechanismsPrimate Behavior and Ecology

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Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns

Petrides, M., Pandya, D. N.·1999·European Journal of Neuroscience

DOI 10.1046/j.1460-9568.1999.00518.x

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Abstract

The cytoarchitecture of the human and the macaque monkey dorsolateral prefrontal cortex has been examined in a strictly comparative manner in order to resolve major discrepancies between the available segmentations of this cortical region in the human and the monkey brain. In addition, the connections of the dorsolateral prefrontal cortical areas were re‐examined in the monkey. The present analysis showed that only a restricted portion of what had previously been labelled as area 46 in the monkey has the same characteristics as area 46 of the human brain; the remaining part of this monkey region has the characteristics of a portion of the middle frontal gyrus in the human brain that had previously been included as part of area 9. We have labelled this cortical area as 9/46 in both species. These two areas (i.e. 46 and 9/46), which constitute the lower half of the mid‐dorsolateral frontal cortex, have a well‐developed granular layer IV, and can easily be distinguished from area 9, on the upper part of the mid‐dorsolateral region, which does not have a well‐developed granular layer IV. Area 9 has the same basic pattern of connections as areas 46 and 9/46, but, unlike the latter areas, it does not receive input from the lateral parietal cortex. Caudal to area 9, on the dorsomedial portion of the frontal cortex, there is a distinct strip of cortex (area 8B) which, unlike area 9, receives significant input from the prestriate cortex and the medial parietal cortex. The present results provide a basis for a closer integration of findings from functional neuroimaging studies in human subjects with experimental work in the monkey.

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Cingulate and cerebellar beta oscillations are engaged in the acquisition of auditory‐motor sequences
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“There is, however, growing evidence that cingulate regions posterior to the ACC—the PCC—also have a crucial role during errormonitoring [Agam et al, 2011; Heilbronner and Platt, 2013] and are affected by error agency [de Bruijn et al. 2009].”
BackgroundInfluential
Functional rostro-caudal gradient in the human posterior lateral frontal cortex
Amiez, C., & Petrides, M. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1567-z · Cited by 32
Self-citation
Disrupted interactions among the hippocampal, dorsal attention, and central‐executive networks in amnestic mild cognitive impairment
Chand, G. B., Hajjar, I. M., & Qiu, D. (2018) · Human Brain Mapping · doi:10.1002/hbm.24339 · Cited by 28
“…cortices in several cognitive functions, such as integrating information from the external environment with the stored internal representation during executive decision-making processes (Chand & Dhamala, 2017; Chand, Lamichhane, & Dhamala, 2016; Miller & Cohen, 2001; Petrides & Pandya, 1999).”
Background
The Basal Ganglia
Haber, S. N., & Gdowski, M. (2004) · Elsevier eBooks · doi:10.1016/b978-012547626-3/50022-3 · Cited by 33
Targeting suicidal ideation in major depressive disorder with MRI-navigated Stanford accelerated intelligent neuromodulation therapy
Baojuan Li, A., Zhao, N., Tang, N., Friston, K. J., Zhai, W., Wu, D., Liu, J., Chen, Y., Yan, M., Qiao, Y., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-023-02707-9 · Cited by 34
“Anatomically, previous studies have reported the absence of direct anatomical connections between BA46 (DLPFC) and BA25 (sgACC) [60].”
Background
Impairment only on the fluency subtest of the Frontal Assessment Battery after prefrontal lesions.
Chapados, C., & Petrides, M. (2013) · Brain : a journal of neurology · doi:10.1093/brain/awt228 · Cited by 32
Self-citation
Computing Social Value Conversion in the Human Brain
Fukuda, H., Ma, N., Suzuki, S., Harasawa, N., Ueno, K., Gardner, J. L., Ichinohe, N., Haruno, M., Cheng, K., & Nakahara, H. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.3117-18.2019 · Cited by 35
“These findings are corroborated by previous findings regarding these regions’ functional and anatomical connections (Petrides and Pandya, 1999; Ongür and Price, 2000; Mars et al., 2013; Schmidt et al., 2018).”
Result
Parcellation-based tractographic modeling of the ventral attention network
Allan, P. G., Briggs, R. G., Conner, A. K., O’Neal, C. M., Bonney, P. A., Maxwell, B. D., Baker, C. M., Burks, J. D., Sali, G., Glenn, C. A., et al. (2019) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2019.116548 · Cited by 32
Neuronal activity in the primate dorsomedial prefrontal cortex contributes to strategic selection of response tactics
Matsuzaka, Y., Akiyama, T., Tanji, J., & Mushiake, H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119971109 · Cited by 32
“The contributions of the pmPFC and dlPFC, which have different afferent inputs (1), to rule-based behavioral control may differ considerably (36).”
Background
Presurgical Mapping of Verbal Language in Brain Tumors with Functional MR Imaging and MR Tractography
Bizzi, A. (2009) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2009.08.010 · Cited by 32
Functional imaging of the auditory processing applied to speech sounds
Patterson, R. D., & Johnsrude, I. S. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2157 · Cited by 32
Emotion regulation related neural predictors of cognitive behavioral therapy response in social anxiety disorder
Klumpp, H., Roberts, J., Kennedy, A. E., Shankman, S. A., Langenecker, S. A., Gross, J. J., & Phan, K. L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.01.010 · Cited by 34
“…area well-positioned to integrate sensory information and behavioral control given its interconnections with other prefrontal areas (Miller and Cohen, 2001), motor regions (e.g., supplementary motor area) (Petrides and Pandya, 1999), and input from parietal areas (Petrides and Pandya, 1999).”
Review of EEG Affective Recognition with a Neuroscience Perspective
Lim, R. Y., Lew, W.-C. L., & Ang, K. K. (2024) · Brain Sciences · doi:10.3390/brainsci14040364 · Cited by 38
“Apart from its extensive association with brain regions providing sensory inputs such as occipital, temporal, and parietal cortices [55–57], the PFC also has anatomical connections with brain regions that are sites of input integration.”
Background
The connectivity of the human frontal pole cortex, and a theory of its involvement in exploit versus explore
Rolls, E. T., Deco, G., Huang, C., & Feng, J. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad416 · Cited by 31
Memory consolidation in humans: new evidence and opportunities
Maguire, E. A. (2014) · Experimental Physiology · doi:10.1113/expphysiol.2013.072157 · Cited by 36
Rules through Recursion: How Interactions between the Frontal Cortex and Basal Ganglia May Build Abstract, Complex Rules from Concrete, Simple Ones
Miller, E. K., & Buschman, T. J. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195314274.003.0022 · Cited by 33
“, 1991; Petrides and Pandya, 1999).”
Evolution of regulatory signatures in primate cortical neurons at cell-type resolution
Kozlenkov, A., Vermunt, M. W., Apontes, P., Li, J., Hao, K., Sherwood, C. C., Hof, P. R., Ely, J. J., Wegner, M., Mukamel, E. A., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2011884117 · Cited by 30
“The DLPFC was sampled from frozen brains in a region corresponding to BA9 as described in macaques and chimpanzees (74).”
Method
The dual origin hypothesis: An evolutionary brain-behavior framework for analyzing psychiatric disorders
Giaccio, R. G. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.021 · Cited by 34
Cyto-, myelo- and chemoarchitecture of the prefrontal cortex of the Cebus monkey
Cruz-Rizzolo, R., de Lima, M. A., Ervolino, E., de Oliveira, J. A. D., & Casatti, C. (2011) · BMC Neuroscience · doi:10.1186/1471-2202-12-6 · Cited by 33
“Area 32c, rostral to the corpus callosum, partly corresponds to the macaque area 32 of Barbas and Pandya [25], Vogt et al. [39] and Carmichael and Price [27] (Figure 1C), and area PL of Preuss and Goldman-Rakic [5].”
BackgroundResultInfluential
Cortical Afferents and Myeloarchitecture Distinguish the Medial Intraparietal Area (MIP) from Neighboring Subdivisions of the Macaque Cortex
Bakola, S., Passarelli, L., Huynh, T., Impieri, D., Worthy, K. H., Fattori, P., Galletti, C., Burman, K. J., & Rosa, M. G. P. (2017) · eNeuro · doi:10.1523/eneuro.0344-17.2017 · Cited by 33
“The few labeled cells in the dorsolateral prefrontal cortex, near and in the principal sulcus, were attributed to areas 9/46 (Petrides and Pandya, 1999).”
Background
Different macaque models of cognitive aging exhibit task-dependent behavioral disparities
Comrie, A. E., Gray, D. T., Smith, A. C., & Barnes, C. A. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.02.008 · Cited by 30
Behavioral flexibility is associated with changes in structure and function distributed across a frontal cortical network in macaques
Sallet, J., Noonan, M. P., Thomas, A. G., O’Reilly, J. X., Anderson, J., Papageorgiou, G., Neubert, F. X., Ahmed, B., Smith, J. E. T., Bell, A. H., et al. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000605 · Cited by 29
“The co-recruitment of plOFC/AI and another region near to, but outside, central OFC, lOFC/12o, may reflect direct connections between the areas [69,70].”
Background
Cytoarchitecture and Maps of the Human Cerebral Cortex
Zilles, K., Palomero‐Gallagher, N., & Amunts, K. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397025-1.00207-4 · Cited by 31
Oscillatory activity in prefrontal and posterior regions during implicit letter-location binding
Campo, P., Poch, C., Parmentier, F. B. R., Moratti, S., Elsley, J. V., Castellanos, N. P., Ruiz-Vargas, J. M., del Pozo, F., & Maestú, F. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.024 · Cited by 30
“Furthermore , neurons coding different types of information are intermingled in the prefrontal cortex (Petrides and Pandya, 1999; Wilson et al., 1993).”
Multivariate Granger Causality Analysis of Acupuncture Effects in Mild Cognitive Impairment Patients: An fMRI Study
Chen, S., Bai, L., Xu, M., Wang, F., Yin, L., Peng, X., Chen, X., & Shi, X. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/127271 · Cited by 30
“TheDLPFC plays a role in sustaining attention and working memory [46, 47].”
Background
Late-onset hypersensitivity after a lesion in the ventral posterolateral nucleus of the thalamus: A macaque model of central post-stroke pain
Nagasaka, K., Takashima, I., Matsuda, K., & Higo, N. (2017) · Scientific Reports · doi:10.1038/s41598-017-10679-2 · Cited by 30
Cortical chemoarchitecture shapes macroscale effective functional connectivity patterns in macaque cerebral cortex
Turk, E., Scholtens, L. H., & van den Heuvel, M. P. (2016) · Human Brain Mapping · doi:10.1002/hbm.23141 · Cited by 27
“Pandya et al. showed in the macaque and human cortex that distinct cytoarchitectonic sub-regions have unique patterns of corticocortical connectivity [Pandya and Sanides, 1973; Petrides and Pandya, 1999, 2002].”
Diverse Synaptic Distributions of G Protein-coupled Estrogen Receptor 1 in Monkey Prefrontal Cortex with Aging and Menopause
Crimins, J. L., Wang, A. C., Yuk, F., Puri, R., Janssen, W. G. M., Hara, Y., Rapp, P. R., & Morrison, J. H. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw050 · Cited by 29
Inhibition of Lateral Prefrontal Cortex Produces Emotionally Biased First Impressions: A Transcranial Magnetic Stimulation and Electroencephalography Study
Lapate, R. C., Samaha, J., Rokers, B., Hamzah, H., Postle, B. R., & Davidson, R. J. (2017) · Psychological Science · doi:10.1177/0956797617699837 · Cited by 29
“This lPFC region, near the inferior frontal sulcus, is estimated to be in Brodmann’s area 9/46v (Petrides & Pandya, 1999), and is highly interconnected with the frontoparietal network, multimodal temporal cortex, and cingulate cortex (Petrides & Pandya, 1999).”
Background
Efficacy of rTMS in decreasing postnatal depression symptoms: A systematic review.
Ganho-Ávila, A., Poleszczyk, A., Mohamed, M. M. A., & Osorio, A. (2019) · Psychiatry Research · doi:10.1016/j.psychres.2019.05.042 · Cited by 27
Using Tertiary Sulci to Map the “Cognitive Globe” of Prefrontal Cortex
Miller, J. A., D’Esposito, M., & Weiner, K. S. (2021) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01696 · Cited by 31
Architectonic mapping of the medial region of the human orbitofrontal cortex by density profiles.
Mackey, S., & Petrides, M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.036 · Cited by 27
Self-citation
‘Do I like this person?’ A network analysis of midline cortex during a social preference task
Chen, A. C., Welsh, R. C., Liberzon, I., & Taylor, S. F. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.02.044 · Cited by 30
“Group analysis of task effects Relative to the resting baseline, both Preference and Gender tasks recruited: 1) Increased activity in a set of brain regions typically seen for perceptual processing and task execution, including: occipital lobe (fusiform face areas, FFA, included), precentral gyrus, dACC, pre-SMA, bila…”
BackgroundInfluential
A role for the serotonin 2A receptor in the expansion and functioning of human transmodal cortex
Luppi, A. I., Girn, M., Rosas, F. E., Timmermann, C., Roseman, L., Erritzøe, D., Nutt, D., Stamatakis, E. A., Spreng, R. N., Xing, L., et al. (2023) · Brain · doi:10.1093/brain/awad311 · Cited by 31
Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex
Kwok, S. C., Cai, Y., & Buckley, M. J. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.0330-19.2019 · Cited by 28
“When referring to cytoarchitecturally defined regions in the lesion description below, we have adopted the nomenclature and conventions of Petrides and Pandya (1999) and have reconstructed lesion extents on standard drawings based upon those provided by the Laboratory of Neuropsychology at National…”
Method
A preliminary study of association between adolescent estradiol level and dorsolateral prefrontal cortex activity during emotion regulation
Chung, Y. S., Poppe, A. B., Novotny, S. E., Epperson, C. N., Hedy Kober, A., Granger, D. A., Blumberg, H. P., Ochsner, K. N., Gross, J. J., Pearlson, G. D., et al. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104398 · Cited by 32
“, 2016) that most closely corresponded to the cytoarchtectonically-identified lateral prefrontal area 46 in rhesus monkey studies (Petrides and Pandya, 1999).”
Background
Longitudinal Neuroimaging Analysis in Mild-Moderate Alzheimer’s Disease Patients Treated with Plasma Exchange with 5% Human Albumin
Cuberas‐Borrós, G., Roca, I., Boada, M., Tárraga, L., Hernández, I., Buendía, M., Rubio, L., Torres, G., Bittini, A., Guzmán‐De‐Villoria, J. A., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170693 · Cited by 28
“BA 46 corresponds with the dorsolateral prefrontal cortex which plays a role in sustaining attention and working memory [33].”
Background
Brain Metabolic Correlates of Decision Making in Amnestic Mild Cognitive Impairment
Griffith, H. R., Okonkwo, O. C., den Hollander, J. A., Belue, K., Copeland, J., Harrell, L. E., Brockington, J. C., Clark, D. G., & Marson, D. C. (2010) · Aging Neuropsychology and Cognition · doi:10.1080/13825581003646135 · Cited by 28
“The posterior cingulate is known to be interconnected with diverse brain regions involved in higher-order cognition, such as the frontal midline regions ( Braak & Braak, 1993 ), orbitofrontal and dorsolateral prefrontal cortices ( Baleydier & Mauguiere, 1980 ; Petrides & Pandya, 1999 ), and medial temporal lobes ( Bal…”
Background
The Anatomical Segregation of the Frontal Cortex: What Does it Mean for Function?
Amunts, K., & von Cramon, D. Y. (2006) · Cortex · doi:10.1016/s0010-9452(08)70392-7 · Cited by 28
Time Modulated Prefrontal and Parietal Activity during the Maintenance of Integrated Information as Revealed by Magnetoencephalography
Campo, P. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh115 · Cited by 29
“The anatomical connectivity between SFG and SPL has been reported in several studies ( Petrides and Pandya, 1999; Petrides, 2000b).”
Background
Functional Specialization within Macaque Dorsolateral Prefrontal Cortex for the Maintenance of Task Rules and Cognitive Control
Hussein, S., Johnston, K., Belbeck, B., Lomber, S. G., & Everling, S. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00608 · Cited by 27
A frontal lobe surface analysis in three archaic African human fossils: OH 9, Buia, and Bodo
Beaudet, A., & Bruner, E. (2017) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2016.12.002 · Cited by 27
Neuroimmune nexus of depression and dementia: Shared mechanisms and therapeutic targets
Herman, F. J., Simkovic, S. J., & Pasinetti, G. M. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14569 · Cited by 29
Resting-state functional connectivity in medication-naïve adolescents with major depressive disorder
Lee, J., Pavuluri, M. N., Kim, J. H., Suh, S., Kim, I. S., & Lee, M. (2019) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2019.04.008 · Cited by 27
Side-by-side regions in dorsolateral prefrontal cortex estimated within the individual respond differentially to domain-specific and domain-flexible processes
DiNicola, L. M., Sun, W., & Buckner, R. L. (2023) · Journal of Neurophysiology · doi:10.1152/jn.00277.2023 · Cited by 28
“Petrides and Pandya (68) replicated, across multiple rhesus monkey cases, that injections at or near area 9/46d in PFC label parahippocampal gyrus.”
Background
Anomalous Cerebellar Anatomy in Chinese Children with Dyslexia
Yang, Y., Yang, Y., Chen, B., Zhang, Y.-W., & Bi, H. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00324 · Cited by 27
“…showed in the scatter plot, the black line represents the correlation line for all participants. with the dorsolateral prefrontal cortex (BA 9/46) (Petrides and Pandya, 1999; Middleton and Strick, 2001), and inferotemporal and posterior parietal cortices (BA 7) (Ramnani, 2006; Jissendi et al.,…”
Background
The neural basis of language talent in bilinguals
Perani, D. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.03.001 · Cited by 27
Task-relevant Output Signals are Sent from Monkey Dorsolateral Prefrontal Cortex to the Superior Colliculus during a Visuospatial Working Memory Task
Johnston, K., & Everling, S. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21067 · Cited by 28
“These signals share a great deal of similarity with those we observed in DLPFC cortico-tectal neurons, suggesting that there is substantial overlap in the signals sent from the FEF, LIP, and DLPFC to the SC. This is perhaps not surprising given the extensive interconnections between these areas ( Petrides & Pandya, 19…”
Result

Authors: Petrides, M., & Pandya, D. N.
Affiliations: Montreal Neurological Institute and Hospital (CA)
Corresponding author: Petrides, M.
ORCID: Petrides, M.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 1999-03
Volume: 11
Issue: 3
Pages: 1011-1036
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1046/j.1460-9568.1999.00518.x
OpenAlex: W1965597399
Cited by: 1,068
References: 43
Citations by year: 2026: 25 · 2025: 26 · 2024: 34 · 2023: 27 · 2022: 29 · 2021: 37 · 2020: 37 · 2019: 41 · 2018: 48 · 2017: 63 · 2016: 38 · 2015: 48 · 2014: 45 · 2013: 41 · 2012: 54
FWCI: 10.01
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 1029 d)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Natural Sciences and Engineering Research Council of Canada
Medical Research Council
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
Keywords: dorsolateral prefrontal cortex, cytoarchitecture, human-macaque comparison, area 46, middle frontal gyrus, corticocortical connections, lateral parietal cortex, medial parietal cortex, prestriate cortex
MeSH terms: Animals, Brain Mapping, Humans, Interneurons, Macaca mulatta, Neural Pathways, Prefrontal Cortex

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Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns

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