Skip to main content
Log in

Functional rostro-caudal gradient in the human posterior lateral frontal cortex

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The present study examined the hypothesis that the posterior motor/premotor region of the lateral frontal cortex is functionally organized along a rostro-caudal axis. During functional magnetic resonance imaging scanning, the subjects performed various tasks assessing basic saccadic eye or hand actions and also tasks requiring the cognitive selection between competing hand or eye movements based on previously learned conditional relations (if A, select movement X, but if B select movement Y). Subject-by-subject analysis demonstrated precise relationships between the foci of functional activity and specific sulci. In agreement with previous reports, basic eye movements activated the Frontal Eye Field (FEF) in the ventral branch of the superior precentral sulcus, but the high-level selection of saccadic eye movements was localized systematically anterior to this region in the superior frontal sulcus. Similarly, basic performance of hand movements activated the primary motor cortex, but the region involved in the high-level selection between competing hand movements was systematically localized within the dorsal branch of the superior precentral sulcus, anterior to the primary motor region. Importantly, there was no overlap between the anterior cognitive selection regions, suggesting an effector specific organization. These results demonstrate a functional rostro-caudal gradient within the posterior lateral frontal cortex reflecting a hierarchical organization of action control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amiez C, Petrides M (2007) Selective involvement of the mid-dorsolateral prefrontal cortex in the coding of the serial order of visual stimuli in working memory. Proc Natl Acad Sci USA 104:13786–13791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amiez C, Petrides M (2009) Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Prog Neurobiol 89:220–230

    Article  PubMed  Google Scholar 

  • Amiez C, Petrides M (2014) Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas. Cereb Cortex 24:563–578

    Article  PubMed  Google Scholar 

  • Amiez C, Kostopoulos P, Champod AS, Petrides M (2006) Local morphology predicts functional organization of the dorsal premotor region in the human brain. J Neurosci 26:2724–2731

    Article  CAS  PubMed  Google Scholar 

  • Amiez C, Hadj-Bouziane F, Petrides M (2012) Response selection versus feedback analysis in conditional visuo-motor learning. NeuroImage 59(4):3723–3735

    Article  CAS  PubMed  Google Scholar 

  • Amiez C, Neveu R, Warrot D, Petrides M, Knoblauch K, Procyk E (2013) The location of feedback-related activity in the midcingulate cortex is predicted by local morphology. J Neurosci 33:2217–2228

    Article  CAS  PubMed  Google Scholar 

  • Andersen RA, Gnadt JW (1989) Posterior parietal cortex. Rev Oculomot Res 3:315–335

    CAS  PubMed  Google Scholar 

  • Badre D (2008) Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes. Trends Cogn Sci 12:193–200

    Article  PubMed  Google Scholar 

  • Badre D, D’Esposito M (2007) Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J Cogn Neurosci 19:2082–2099

    Article  PubMed  Google Scholar 

  • Badre D, D’Esposito M (2009) Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci 10:659–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badre D, Hoffman J, Cooney JW, D’Esposito M (2009) Hierarchical cognitive control deficits following damage to the human frontal lobe. Nat Neurosci 12:515–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botvinick MM (2007) Multilevel structure in behaviour and in the brain: a model of Fuster’s hierarchy. Philos Trans R Soc Lond B Biol Sci 362:1615–1626

    Article  PubMed  PubMed Central  Google Scholar 

  • Buckner RL (2003) Functional-anatomic correlates of control processes in memory. J Neurosci 23:3999–4004

    CAS  PubMed  Google Scholar 

  • Burman KJ, Palmer SM, Gamberini M, Rosa MG (2006) Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas. J Comp Neurol 495:149–172

    Article  PubMed  Google Scholar 

  • Derrfuss J, Vogt VL, Fiebach CJ, von Cramon DY, Tittgemeyer M (2012) Functional organization of the left inferior precentral sulcus: dissociating the inferior frontal eye field and the inferior frontal junction. NeuroImage 59:3829–3837

    Article  CAS  PubMed  Google Scholar 

  • Friston KJ, Frith CD, Turner R, Frackowiak RS (1995a) Characterizing evoked hemodynamics with fMRI. NeuroImage 2:157–165

    Article  CAS  PubMed  Google Scholar 

  • Friston KJ, Frith CD, Frackowiak RS, Turner R (1995b) Characterizing dynamic brain responses with fMRI: a multivariate approach. NeuroImage 2:166–172

    Article  CAS  PubMed  Google Scholar 

  • Friston KJ, Holmes AP, Poline JB, Grasby PJ, Williams SC, Frackowiak RS, Turner R (1995c) Analysis of fMRI time-series revisited. NeuroImage 2:45–53

    Article  CAS  PubMed  Google Scholar 

  • Goulas A, Uylings HB, Stiers P (2012) Unravelling the intrinsic functional organization of the human lateral frontal cortex: a parcellation scheme based on resting state fMRI. J Neurosci 32:10238–10252

    Article  CAS  PubMed  Google Scholar 

  • Grosbras MH, Laird AR, Paus T (2005) Cortical regions involved in eye movements, shifts of attention, and gaze perception. Hum Brain Mapp 25:140–154

    Article  PubMed  Google Scholar 

  • Koechlin E, Ody C, Kouneiher F (2003) The architecture of cognitive control in the human prefrontal cortex. Science 302:1181–1185

    Article  CAS  PubMed  Google Scholar 

  • Koyama M, Hasegawa I, Osada T, Adachi Y, Nakahara K, Miyashita Y (2004) Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41:795–807

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Sescousse G, Amiez C, Dreher JC (2015) Local morphology predicts functional organization of experienced value signals in the human orbitofrontal cortex. J Neurosci 35(4):1648–1658

    Article  CAS  PubMed  Google Scholar 

  • Luppino G, Rozzi S, Calzavara R, Matelli M (2003) Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur J Neurosci 17:559–578

    Article  PubMed  Google Scholar 

  • Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S, Squatrito S, Molinari M, Lacquaniti F, Caminiti R (2001) Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 11:513–527

    Article  CAS  PubMed  Google Scholar 

  • Matelli M, Govoni P, Galletti C, Kutz DF, Luppino G (1998) Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J Comp Neurol 402:327–352

    Article  CAS  PubMed  Google Scholar 

  • Miller LM, D’Esposito M (2005) Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. J Neurosci 25:5884–5893

    Article  CAS  PubMed  Google Scholar 

  • Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871–908

    Article  CAS  PubMed  Google Scholar 

  • O’Reilly RC (2006) Biologically based computational models of high-level cognition. Science 314:91–94

    Article  PubMed  Google Scholar 

  • O’Reilly RC, Noelle DC, Braver TS, Cohen JD (2002) Prefrontal cortex and dynamic categorization tasks: representational organization and neuromodulatory control. Cereb Cortex 12:246–257

    Article  PubMed  Google Scholar 

  • Paus T (1996) Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34:475–483

    Article  CAS  PubMed  Google Scholar 

  • Petrides M (1982) Motor conditional associative learning after selective prefrontal lesions in the monkey. Behav Brain Res 5:407–413

    Article  CAS  PubMed  Google Scholar 

  • Petrides M (1985) Deficits on conditional associative-learning task after frontal- and temporal-lobe lesions in man. Neuropsychologia 23:601–614

    Article  CAS  PubMed  Google Scholar 

  • Petrides M (1997) Visuo-motor conditional associative learning after frontal and temporal lesions in the human brain. Neuropsychologia 35:989–997

    Article  CAS  PubMed  Google Scholar 

  • Petrides M (2005a) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci 360:781–795

    Article  PubMed  PubMed Central  Google Scholar 

  • Petrides M (2005b) The rostral-caudal axis of cognitive control within the lateral frontal cortex. In: Dehaene S, Duhamel J-R, Hauser MD, Rizzolatti G (eds) From monkey to human brain. MIT, Cambridge, pp 293–314

    Google Scholar 

  • Petrides M, Pandya DN (1984) Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J Comp Neurol 228:105–116

    Article  CAS  PubMed  Google Scholar 

  • Petrides M, Pandya DN (1999) Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur J Neurosci 11:1011–1036

    Article  CAS  PubMed  Google Scholar 

  • Procyk E, Wilson C, Stoll F, Faraut M, Petrides M, Amiez C (2015) Midcingulate motor map and feedback detection: converging data from humans and monkeys. Cereb Cortex. https://doi.org/10.1093/cercor/bhu213

    Google Scholar 

  • Sallet J, Mars RB, Noonan MP, Neubert FX, Jbabdi S, O’Reilly JX, Filippini N, Thomas AG, Rushworth MF (2013) The organization of dorsal frontal cortex in humans and macaques. J Neurosci 33:12255–12274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segal E, Petrides M (2013) Functional activation during reading in relation to the sulci of the angular gyrus region. Eur J Neurosci 38:2793–2801

    Article  PubMed  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York

  • Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58–73

    Article  CAS  PubMed  Google Scholar 

  • Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus A new landmark. Brain 120(Pt 1):141–157

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The research was supported by Canadian Institutes of Health Research (CIHR) grant FRN 37753 and FDN-143212 to M. Petrides.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Céline Amiez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amiez, C., Petrides, M. Functional rostro-caudal gradient in the human posterior lateral frontal cortex. Brain Struct Funct 223, 1487–1499 (2018). https://doi.org/10.1007/s00429-017-1567-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-017-1567-z

Keywords

Navigation