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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Background
The cortical motor system of the marmoset monkey (Callithrix jacchus)
Bakola, S., Burman, K. J., & Rosa, M. G. P. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.11.003 · Cited by 49
Integration of Cognitive and Motivational Information in the Primate Lateral Prefrontal Cortex
Sakagami, M., & Watanabe, M. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.010 · Cited by 48
Risperidone and Divalproex Differentially Engage the Fronto-Striato-Temporal Circuitry in Pediatric Mania: A Pharmacological Functional Magnetic Resonance Imaging Study
Pavuluri, M. N., Passarotti, A. M., Fitzgerald, J. M., Wegbreit, E., & Sweeney, J. A. (2011) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2011.10.019 · Cited by 49
Disconnection Between Amygdala and Medial Prefrontal Cortex in Psychotic Disorders
Mukherjee, P., Sabharwal, A., Kotov, R., Szekely, A., Parsey, R. V., Barch, D. M., & Mohanty, A. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbw012 · Cited by 52
Rostro-Caudal Organization of Connectivity between Cingulate Motor Areas and Lateral Frontal Regions
Loh, K. K., Hadj‐Bouziane, F., Petrides, M., Procyk, E., & Amiez, C. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00753 · Cited by 49
Self-citation
Evolutional and developmental anatomical architecture of the left inferior frontal gyrus
Wang, J., Yang, Y., Zhao, X., Zuo, Z., & Tan, L. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117268 · Cited by 49
Foraging with the frontal cortex: A cross-species evaluation of reward-guided behavior
Rudebeck, P. H., & Izquierdo, A. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01140-0 · Cited by 55
Encoding of Rules by Neurons in the Human Dorsolateral Prefrontal Cortex
Mian, M. K., Sheth, S. A., Patel, S. R., Spiliopoulos, K., Eskandar, E. N., & Williams, Z. M. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs361 · Cited by 49
Antisaccade Deficit after Inactivation of the Principal Sulcus in Monkeys
Condy, C., Wattiez, N., Rivaud-Péchoux, S., Tremblay, L., & Gaymard, B. M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj140 · Cited by 48
“It overlaps with the caudal part of area 46v/9, which includes the depth of the dorsal bank, the fundus, and most of the ventral bank of the principal sulcus (Barbas and Pandya 1989; Petrides and Pandya 1999 ).”
Background
Acoustic evaluation of short-term effects of repetitive transcranial magnetic stimulation on motor aspects of speech in Parkinson’s disease
Eliasova, I., Mekyska, J., Košťálová, M., Mareček, R., Smékal, Z., & Rektorová, I. (2012) · Journal of Neural Transmission · doi:10.1007/s00702-012-0953-1 · Cited by 49
“These coordinates were chosen based on the probable DLPFC location as revealed by a PET study of verbal working memory (Petrides et al. 1993) and used by other authors (Strafella et al. 2001; Barrett et al. 2004), corresponding to cytoarchitectonic area 9/46 as defined by Petrides and Pandya (1999).”
Method
Interactions between the anterior cingulate-insula network and the fronto-parietal network during perceptual decision-making
Chand, G. B., & Dhamala, M. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.014 · Cited by 47
Prefrontal contributions to the stability and variability of thought and conscious experience
Zamani, A., Carhart-Harris, R. L., & Kalina Christoff, A. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01147-7 · Cited by 49
“Second, the mOFC is anatomically connected to brain regions that likely provide it with access to information about different goals and needs, including: lateral prefrontal regions [174, 175, 226, 227] for task context and long-term goals [119, 122], the anterior medial PFC [227, 228] for self-relevance and personal s…”
Background
Differences and Similarities on Neuronal Activities of People Being Happily and Unhappily in Love: A Functional Magnetic Resonance Imaging Study
Stoessel, C., Stiller, J., Bleich, S., Boensch, D., Doerfler, A., Garcia, M., Richter‐Schmidinger, T., Kornhuber, J., & Forster, C. (2011) · Neuropsychobiology · doi:10.1159/000325076 · Cited by 47
Identification and disruption of a neural mechanism for accumulating prospective metacognitive information prior to decision-making
Miyamoto, K., Trudel, N., Kamermans, K., Lim, M. C., Lazari, A., Verhagen, L., Wittmann, M. K., & Rushworth, M. F. S. (2021) · Neuron · doi:10.1016/j.neuron.2021.02.024 · Cited by 45
“In the vicinity of the alPFC47 and FPm (20-mm radius centered on either area), individual variation in activity of the alPFC close to area 46 (Petrides and Pandya, 1999) was correlated with individual variation in metacognitive accuracy (type II AROC) (Figure 6B), whereas individual variation in FPmand vmPFC (area 11m…”
Background
A Proposed Number System for the 107 Cortical Areas of Economo and Koskinas, and Brodmann Area Correlations
Triarhou, L. C. (2007) · Stereotactic and Functional Neurosurgery · doi:10.1159/000103259 · Cited by 46
The different faces of one's self: An fMRI study into the recognition of current and past self-facial appearances
Apps, M. A. J., Tajadura‐Jiménez, A., Turley, G., & Manos Tsakiris, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.08.053 · Cited by 47
Lateral Prefrontal Cortex is Organized into Parallel Dorsal and Ventral Streams Along the Rostro-Caudal Axis
Blumenfeld, R. S., Nomura, E. M., Gratton, C., & D’Esposito, M. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs223 · Cited by 48
Evidence for a Functional Hierarchy of Association Networks
Choi, E. Y., Drayna, G. K., & Badre, D. (2018) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01229 · Cited by 43
“…studies show that the LFC has widespread connections to regions in frontal, parietal, and temporal association cortices (Saleem, Miller, & Price, 2014; Morecraft et al., 2012; Petrides & Pandya, 1999, 2006;Morecraft,Geula,&Mesulam, 1992; Cavada & Goldman-Rakic, 1989a, 1989b; Vogt & Pandya, 1987).”
Background
Perceptual metacognition of human faces is causally supported by function of the lateral prefrontal cortex
Lapate, R. C., Samaha, J., Rokers, B., Postle, B. R., & Davidson, R. J. (2020) · Communications Biology · doi:10.1038/s42003-020-1049-3 · Cited by 50
“(27)) largely support the latter viewpoint, wherein LPFC reads out the strength of sensory information from lower-order cortices, which is consistent with the extensive connectivity between frontoparietal and multimodal temporal cortex (36).”
BackgroundResult
fMRI investigation of speed–accuracy strategy switching
Vallesi, A., McIntosh, A. R., Crescentini, C., & Stuss, D. T. (2011) · Human Brain Mapping · doi:10.1002/hbm.21312 · Cited by 46
“The fronto-medial wall, and in particular the anterior cingulate, has intensive reciprocal connections with the DLPFC [Bates and Goldman-Rakic, 1993; Petrides and Pandya, 1999].”
Method
Neural foundations of overt and covert actions
Simos, P. G., Kavroulakis, E., Maris, T. G., Papadaki, E. Z., Boursianis, T., Kalaitzakis, G., & Savaki, H. E. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.036 · Cited by 47
“This finding is compatible with reports that the dorsolateral prefrontal cortex plays a role in sustaining attention and working memory (Petrides and Pandya, 1999; Zhang et al., 2003) while overriding automatic responses (Kubler et al.”
Result
Multivariate Granger causality unveils directed parietal to prefrontal cortex connectivity during task-free MRI
Duggento, A., Passamonti, L., Valenza, G., Barbieri, R., Guerrisi, M., & Toschi, N. (2018) · Scientific Reports · doi:10.1038/s41598-018-23996-x · Cited by 45
The Moral Brain
Verplaetse, J., Schrijver, J. D., Vanneste, S., & Braeckman, J. (2009) · Springer eBooks · doi:10.1007/978-1-4020-6287-2 · Cited by 49
Multisynaptic projections from the ventrolateral prefrontal cortex to the dorsal premotor cortex in macaques – anatomical substrate for conditional visuomotor behavior
Takahara, D., Inoue, K., Hirata, Y., Miyachi, S., Nambu, A., Takada, M., & Hoshi, E. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08251.x · Cited by 46
“In particular, the dorsal aspect of the principal sulcus and area 8 were subdivided according to Petrides & Pandya (1999) except that the periprincipal area dorsal to the fundus of the principal sulcus was considered a single area (area 46d), and the ventral aspect of the principal sulcus was…”
Method
Visual activation of frontal cortex: segregation from occipital activity
Saron, C. D., Schroeder, C. E., Foxe, J. J., & Vaughan, H. G. (2001) · Cognitive Brain Research · doi:10.1016/s0926-6410(01)00036-2 · Cited by 44
Single-neuron theory of consciousness
Sevush, S. (2005) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2005.06.018 · Cited by 43
An evolutionary approach to art and aesthetic experience.
Zaidel, D. W., Nadal, M., Flexas, A., & Munar, E. (2013) · Psychology of Aesthetics Creativity and the Arts · doi:10.1037/a0028797 · Cited by 44
“…areas, as well as the representation of objects and the processing of symmetry (Bell, Hadj-Bouziane, Frihauf, Tootell, & Ungerleider, 2009; Leichnetz, 2001; Orban, Van Essen, & Vanduffel, 2004; Petrides & Pandya, 1999, 2001; Semendeferi, Armstrong, Schleicher, Zilles, & Van Hoesen, 1998, 2001).”
Species-specific distributions of tyrosine hydroxylase–immunoreactive neurons in the prefrontal cortex of anthropoid primates
Raghanti, M. A., Spocter, M. A., Stimpson, C. D., Erwin, J. M., Bonar, C. J., Allman, J. M., Hof, P. R., & Sherwood, C. C. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.058 · Cited by 42
“Cytoarchitectural features were relied upon for identification of cortical regions due to individual variation in their gross anatomical location (e.g. Amunts et al., 1996; Petrides and Pandya, 1999; Rademacher et al., 2001; Zilles et al., 1996).”
Influential
Neural cognitive signals during spontaneous movements in the macaque
Tremblay, S., Testard, C., DiTullio, R. W., Inchauspé, J., & Petrides, M. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01220-4 · Cited by 41
Self-citation
Cortical and thalamic projections to cytoarchitectural areas 6Va and 8C of the marmoset monkey: Connectionally distinct subdivisions of the lateral premotor cortex
Burman, K. J., Bakola, S., Richardson, K. E., Yu, H., Reser, D. H., & Rosa, M. G. P. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23734 · Cited by 41
“…and Pandya, 1987; Huerta et al., 1987; Arikuni et al., 1988; Barbas, 1988; Deacon, 1992; Kurata, 1991; Ghosh and Gattera, 1995; Lu et al., 1994; Petrides and Pandya, 1999, 2002; Wang et al., 2002; Stanton et al., 2005; Gharbawie et al., 2011a), rostral parietal somatosensory areas (e.g., areas…”
Background
Lexicality drives audio-motor transformations in Broca’s area
Kotz, S. A., D’Ausilio, A., Raettig, T., Begliomini, C., Craighero, L., Fabbri‐Destro, M., Zingales, C., Haggard, P., & Fadiga, L. (2009) · Brain and Language · doi:10.1016/j.bandl.2009.07.008 · Cited by 46
“More interestingly, from a cytoarchitectonical point of view, this area closely resembles monkey pre-motor area F5 (Petrides, Cadoret, & Mackey, 2005; Petrides and Pandya, 1999), where mirror neurons have been found.”
Background
Electrophysiological signatures of spontaneous BOLD fluctuations in macaque prefrontal cortex
Hutchison, R. M., Hashemi, N., Gati, J. S., Menon, R. S., & Everling, S. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.03.062 · Cited by 43
“The pattern is consistent with our earlier work in a larger sample of monkeys (caudal cluster in Hutchison and Everling, 2013) and reflective of results from tract-tracing investigations (Petrides and Pandya, 1999).”
BackgroundMethodResultInfluential
Increased MEG activation in OCD reflects a compensatory mechanism specific to the phase of a visual working memory task
Ciesielski, K. T. R., Hämäläinen, M., Lesnik, P. G., GELLER, D. A., & Ahlfors, S. P. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.10.018 · Cited by 43
What saccadic eye movements tell us about TMS-induced neuromodulation of the DLPFC and mood changes: a pilot study in bipolar disorders
Beynel, L., Chauvin, A., Guyader, N., Harquel, S., Bougerol, T., Marendaz, C., & Székely, D. L. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00065 · Cited by 44
Rethinking the Use of Neutral Faces as a Baseline in fMRI Neuroimaging Studies of Axis‐I Psychiatric Disorders
Filkowski, M. M., & Haas, B. W. (2016) · Journal of Neuroimaging · doi:10.1111/jon.12403 · Cited by 46
Evidence for the importance of basal ganglia output nuclei in semantic event sequencing: An fMRI study
Tinaz, S., Schendan, H. E., Schön, K., & Stern, C. E. (2005) · Brain Research · doi:10.1016/j.brainres.2005.10.057 · Cited by 43
“In addition to the right DLPFC (Area 9/46 and 46), the left DLPFC (Area 9/46) (Petrides and Pandya, 1999) demonstrated significant activation.”
BackgroundMethod
Advances in AAV technology for delivering genetically encoded cargo to the nonhuman primate nervous system
Campos, L., Arokiaraj, C. M., Chuapoco, M. R., Chen, X., Goeden, N., Gradinaru, V., & Fox, A. S. (2023) · Current Research in Neurobiology · doi:10.1016/j.crneur.2023.100086 · Cited by 42
The role of the right dorsolateral prefrontal cortex in the Tower of London task performance: repetitive transcranial magnetic stimulation study in patients with Parkinson’s disease
Srovnalová, H., Mareček, R., Kubíková, R., & Rektorová, I. (2012) · Experimental Brain Research · doi:10.1007/s00221-012-3255-9 · Cited by 46
“These coordinates were chosen based on the probable DLPFC location as revealed by a PET study of verbal working memory (Petrides et al. 1993) and used by other authors (Strafella et al. 2001; Barrett et al. 2004), corresponding to cytoarchitectonic area 9/46 as defined by Petrides and Pandya (1999).”
Method
Cortico-basal ganglia networks subserving goal-directed behavior mediated by conditional visuo-goal association
Hoshi, E. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00158 · Cited by 42
Cerebral Metabolism, Cognition, and Functional Abilities in Alzheimer Disease
Melrose, R. J., Ettenhofer, M. L., Harwood, D. G., Achamallah, N., Campa, O., Mandelkern, M. A., & Sultzer, D. L. (2011) · Journal of Geriatric Psychiatry and Neurology · doi:10.1177/0891988711405333 · Cited by 42
Looming and receding visual networks in awake marmosets investigated with fMRI
Cléry, J. C., Schaeffer, D. J., Hori, Y., Gilbert, K. M., Hayrynen, L. K., Gati, J. S., Menon, R. S., & Everling, S. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116815 · Cited by 42
“Area 45B exhibits widespread connectivity patterns in macaques including connections with the inferotemporal cortex, sensory association areas, visual areas and posterior parietal cortex (Carmichael and Price, 1996, 1995a; 1995b; Petrides and Pandya, 1999).”
Fronto-temporal dysfunction in schizophrenia: A selective review
John, J. P. (2009) · Indian Journal of Psychiatry · doi:10.4103/0019-5545.55084 · Cited by 43
“The PFC is a heterogeneous region comprising several areas that are distinct at the cytoarchitectural and functional levels.[3,4] The lateral PFC, usually referred to as the dorsolateral PFC (DLPFC) is considered the central executive for cognitive control, whereas the orbital PFC (OPFC) is considered the central exec…”
Background
Functional Connection Between Posterior Superior Temporal Gyrus and Ventrolateral Prefrontal Cortex in Human
Garell, P. C., Bakken, H. E., Greenlee, J. D. W., Volkov, I. O., Reale, R. A., Oya, H., Kawasaki, H., Howard, M. A., & Brugge, J. F. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs220 · Cited by 42

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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