Skip to main content
Log in

Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey

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

Abstract

The caudal part of the macaque ventrolateral prefrontal cortex (VLPF) is part of several functionally distinct domains. In the present study we combined a cyto- and a myeloarchitectonic approach with a chemoarchitectonic approach based on the distribution of SMI-32 and Calbindin immunoreactivity, to determine the number and extent of architectonically distinct areas occupying this region. Several architectonically distinct areas, completely or partially located in the caudal VLPF, were identified. Two areas are almost completely limited to the anterior bank of the inferior arcuate sulcus, a dorsal one—8/FEF—which extends also more dorsally and should represent the architectonic counterpart of the frontal eye field, and a ventral one—45B—which occupies the ventral half of the bank. Two other areas occupy the ventral prearcuate convexity cortex, a caudal one—area 8r—located just rostral to area 8/FEF and a rostral one—area 45A—which extends as far as the inferior frontal sulcus. Area 45A borders dorsally, in the proximity of the principal sulcus, with area 46 and, ventrally, with area 12. The present data show the existence of two distinct prearcuate convexity areas (8r and 45A), extending other architectonic subdivisions of the caudal VLPF and providing a new, multiarchitectonic frame of reference for this region. The present architectonic data, together with other functional and connectional data, suggest that areas 8/FEF, 45B and 8r are part of the oculomotor frontal cortex, while area 45A is a distinct entity of the VLPF domain involved in high-order processing of nonspatial information.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18

Similar content being viewed by others

References

  • Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Mesulam M-M (1981) Organization of afferent input to subdivision of area 8 in the rhesus monkey. J Comp Neurol 200:407–431

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Mesulam MM (1985) Cortical afferent input to the principalis region of the rhesus monkey. Neuroscience 15:619–637

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375

    Article  PubMed  CAS  Google Scholar 

  • Bettio F, Demelio S, Gobbetti E, Luppino G, Matelli M (2001) Interactive 3-D reconstruction and visualization of primates cerebral cortex. Soc Neurosci Abstr Program No. 728.724

  • von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana

    Google Scholar 

  • Brodmann K (1905) Beitraege zur histologischen Lokalisation der Grosshirnrinde. III. Mitteilung. Die Rindenfelder der niederen Affen. J Psychol Neurol 4:177–266

    Google Scholar 

  • Bruce CJ, Goldberg ME (1984) Physiology of the frontal eye fields. Trends Neurosci 7:436–441

    Article  Google Scholar 

  • Bruce CJ, Goldberg ME, Bushnell C, Stanton GB (1985) Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked movements. J Neurophysiol 54:714–734

    PubMed  CAS  Google Scholar 

  • Cadoret G, Bouchard M, Petrides M (2000) Orofacial representation in the rostral bank of the inferior ramus of the arcuate sulcus of the monkey. Soc Neurosci Abstr Program No. 253.13

  • Calzavara R, Zappala A, Rozzi S, Matelli M, Luppino G (2005) Neurochemical characterization of the cerebellar-recipient motor thalamic territory in the macaque monkey. Eur J Neurosci 21:1869–1894

    Article  PubMed  Google Scholar 

  • Campbell MJ, Morrison JH (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205

    Article  PubMed  CAS  Google Scholar 

  • Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366–402

    Article  PubMed  CAS  Google Scholar 

  • Carmichael ST, Price JL (1995a) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641

    Article  PubMed  CAS  Google Scholar 

  • Carmichael ST, Price JL (1995b) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642–664

    Article  PubMed  CAS  Google Scholar 

  • Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994) Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95–116

    Article  PubMed  Google Scholar 

  • Connolly JD, Goodale MA, Cant JS, Munoz DP (2007) Effector-specific fields for motor preparation in the human frontal cortex. NeuroImage 34:1209

    Article  PubMed  Google Scholar 

  • Cusick CG, Seltzer B, Cola M, Griggs E (1995) Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: evidence for subdivisions of superior temporal polysensory cortex. J Comp Neurol 360:513–535

    Article  PubMed  CAS  Google Scholar 

  • DeFelipe J, Hendry SH, Jones EG (1989) High-resolution light and electron microscopic immunohistochemistry of colocalized GABA and calbindin D-28k in somata of double bouquet cell axons of monkey somatosensory cortex. Eur J Neurosci 4:46–60

    Article  Google Scholar 

  • Dombrowski SM, Hilgetag CC, Barbas H (2001) Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb Cortex 11:975–988

    Article  PubMed  CAS  Google Scholar 

  • Galletti C, Gamberini M, Kutz DF, Fattori P, Luppino G, Matelli M (2001) The cortical connections of area V6: an occipito-parietal network processing visual information. Eur J Neurosci 13:1572–1588

    Article  PubMed  CAS  Google Scholar 

  • Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209

    PubMed  CAS  Google Scholar 

  • Gamlin PD, Yoon K (2000) An area for vergence eye movement in primate frontal cortex. Nature 407:1003

    Article  PubMed  CAS  Google Scholar 

  • Geyer S, Zilles K, Luppino G, Matelli M (2000) Neurofilament protein distribution in the macaque monkey dorsolateral premotor cortex. Eur J Neurosci 12:1554–1566

    Article  PubMed  CAS  Google Scholar 

  • Gregoriou GG, Borra E, Matelli M, Luppino G (2006) Architectonic organization of the inferior parietal convexity of the macaque monkey. J Comp Neurol 496:422–451

    Article  PubMed  Google Scholar 

  • Hendry SH, Jones EG, Emson PC, Lawson DE, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467–472

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161–186

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Glezer II, Conde F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77

    Article  PubMed  CAS  Google Scholar 

  • Huerta MF, Kaas JH (1990) Supplementary eye field as defined by intracortical microstimulation: connections in Macaques. J Comp Neurol 293:299–330

    Article  PubMed  CAS  Google Scholar 

  • Huerta MF, Krubitzer LA, Kaas JH (1987) Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. Cortical connections. J Comp Neurol 265:332–361

    Article  PubMed  CAS  Google Scholar 

  • Kondo H, Tanaka K, Hashikawa T, Jones EG (1994) Neurochemical gradients along the monkey occipito-temporal cortical pathway. Neuroreport 5:613–616

    Article  PubMed  CAS  Google Scholar 

  • Kondo H, Tanaka K, Hashikawa T, Jones EG (1999) Neurochemical gradients along monkey sensory cortical pathways: calbindin-immunoreactive pyramidal neurons in layers II and III. Eur J Neurosci 11:4197–4203

    Article  PubMed  CAS  Google Scholar 

  • Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23–32

    Article  PubMed  CAS  Google Scholar 

  • Luppino G, Calzavara R, Rozzi S, Matelli M (2001) Projections from the superior temporal sulcus to the agranular frontal cortex in the macaque. Eur J Neurosci 14:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Luppino G, Belmalih A, Borra E, Gerbella M, Rozzi S (2006) Architectonics and cortical connections of the ventral prearcuate area 45B of the macaque monkey. Soc Neurosci Abstr Program No. 63.2

  • 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 

  • Maioli MG, Squatrito S, SamolskyDekel BG, Sanseverino ER (1998) Corticocortical connections between frontal periarcuate regions and visual areas of the superior temporal sulcus and the adjoining inferior parietal lobule in the macaque monkey. Brain Res 789:118–125

    Article  PubMed  CAS  Google Scholar 

  • Medalla M, Barbas H (2006) Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur J Neurosci 23:161–179

    Article  PubMed  CAS  Google Scholar 

  • Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W, Guldin W, Hadjidimitrakis K, Savaki HE (2004) Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study. J Neurosci 24:5726–5740

    Article  PubMed  CAS  Google Scholar 

  • Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2005) Observing others: multiple action representation in the frontal lobe. Science 310:332–336

    Article  PubMed  CAS  Google Scholar 

  • Nimchinsky EA, Hof PR, Young WG, Morrison JH (1996) Neurochemical, morphologic, and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey. J Comp Neurol 374:136–160

    Article  PubMed  CAS  Google Scholar 

  • O Scalaidhe SP, Wilson FAW, Goldman-Rakic PS (1997) Areal segregation of face-processing neurons in prefrontal cortex. Science 278:1135–1138

    Article  PubMed  CAS  Google Scholar 

  • O Scalaidhe SP, Wilson FAW, Goldman-Rakic PS (1999) Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. Cereb Cortex 9:459–475

    Article  Google Scholar 

  • Passingham RE (1993) The frontal lobe and voluntary action. Oxford University Press, Oxford

    Google Scholar 

  • Passingham RE, Toni I, Rushworth MFS (2000) Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning. Exp Brain Res 133:103–113

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Petrides M, Pandya DN (1988) Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J Comp Neurol 273:52–66

    Article  PubMed  CAS  Google Scholar 

  • Petrides M, Pandya DN (1994) Comparative architectonic analysis of the human and the macaque frontal cortex. In: Boller F, Grafman J (eds) Handbook of neuropsychology. Elsevier, Amsterdam, pp 17–58

    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  PubMed  CAS  Google Scholar 

  • Petrides M, Pandya DN (2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 16:291–310

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM, Goldman-Rakic PS (1989) Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: anatomical evidence for somatic representation in primate frontal association cortex. J Comp Neurol 282:293–316

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM, Goldman-Rakic PS (1991) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the streptisine primate Galago and the anthropoid primate Macaca. J Comp Neurol 310:429–474

    Article  PubMed  CAS  Google Scholar 

  • Romanski LM (2004) Domain specificity in the primate prefrontal cortex. Cogn Affect Behav Neurosci 4:421–429

    Article  PubMed  Google Scholar 

  • Romanski LM, Goldman-Rakic PS (2002) An auditory domain in primate prefrontal cortex. Nat Neurosci 5:15

    Article  PubMed  CAS  Google Scholar 

  • Romanski LM, Bates JF, Goldman-Rakic PS (1999a) Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 403:141–157

    Article  PubMed  CAS  Google Scholar 

  • Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP (1999b) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat neurosci 2:1131–1136

    Article  PubMed  CAS  Google Scholar 

  • Romanski LM, Averbeck BB, Diltz M (2005) Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurophysiol 93:734–747

    Article  PubMed  Google Scholar 

  • Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M, Luppino G (2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16:1389–1417

    Article  PubMed  Google Scholar 

  • Schall JD, Morel A, King DJ, Bullier J (1995) Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J Neurosci 15:4464–4487

    PubMed  CAS  Google Scholar 

  • Seltzer B, Pandya DN (1989) Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 281:97–113

    Article  PubMed  CAS  Google Scholar 

  • Stanton GB, Deng S-Y, Goldberg ME, McMullen NT (1989) Cytoarchitectural characteristics of the frontal eye fields in macaque monkeys. J Comp Neurol 282:415–427

    Article  PubMed  CAS  Google Scholar 

  • Stanton GB, Bruce CJ, Goldberg ME (1993) Topography of projections to the frontal lobe from the macaque frontal eye fields. J Comp Neurol 330:286–301

    Article  PubMed  CAS  Google Scholar 

  • Stanton GB, Bruce CJ, Goldberg ME (1995) Topography of projections to posterior cortical areas from the macaque frontal eye fields. J Comp Neurol 353:291–305

    Article  PubMed  CAS  Google Scholar 

  • Sugihara T, Diltz MD, Averbeck BB, Romanski LM (2006) Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex. J Neurosci 26:11138–11147

    Article  PubMed  CAS  Google Scholar 

  • Walker E (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 98:59–86

    Article  Google Scholar 

  • Wang Y, Isoda M, Matsuzaka Y, Shima K, Tanji J (2005) Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey. Neurosci Res 53:1

    Article  PubMed  Google Scholar 

  • Watson DE (1992) Contouring: a guide to the analysis and display of spatial data. Pergamon (Elsevier), Tarrytown

    Google Scholar 

  • Wilson FA, Scalaidhe SP, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:1955–1958

    Article  PubMed  CAS  Google Scholar 

  • Zaksas D, Pasternak T (2006) Directional signals in the prefrontal cortex and in area MT during a working memory for visual motion task. J Neurosci 26:11726–11742

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by MIUR (PRIN 2006, no. 2006052343_002). A.B. is supported by a fellowship from EU (Marie Curie, Early stage training program “Sensoprim” MEST-CT-2004-007825). The 3D reconstruction software was developed by CRS4, Pula, Cagliari, Italy. We thank L. Riggio and L. Bonini for valuable help in the statistical analysis and W. Depuydt for developing warping software.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Luppino.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gerbella, M., Belmalih, A., Borra, E. et al. Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey. Brain Struct Funct 212, 269–301 (2007). https://doi.org/10.1007/s00429-007-0158-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-007-0158-9

Keywords

Navigation