Brain Structure and Function

, Volume 221, Issue 1, pp 59–78 | Cite as

Connections of the macaque Granular Frontal Opercular (GrFO) area: a possible neural substrate for the contribution of limbic inputs for controlling hand and face/mouth actions

  • Marzio Gerbella
  • Elena Borra
  • Stefano Rozzi
  • Giuseppe Luppino
Original Article


We traced the connections of the macaque Granular Frontal Opercular (GrFO) area, located in the rostralmost part of the frontal opercular margin, and compared them with those of the caudally adjacent dorsal opercular (DO) and precentral opercular (PrCO) areas. Area GrFO displays strong connections with areas DO, PrCO, and ventrolateral prefrontal (VLPF) area 12l, and even more with the mostly hand-related ventral premotor (PMv) area F5a. Other connections involve the mostly face/mouth-related PMv area F5c, the arm-related area F6/pre-SMA, the hand-related fields of VLPF areas 46v and 12r, and area SII, mostly the hand representation. Furthermore, area GrFO shows rich connectivity with several components of the limbic system including orbitofrontal areas 12o, 12m, and 11, the agranular and dysgranular insula, the agranular cingulate area 24, and the amygdala. Thalamic afferents originate primarily from the parvocellular and the magnocellular subdivisions of the mediodorsal nucleus and from midline and intralaminar nuclei. This connectivity pattern clearly distinguishes area GrFO from areas DO and PrCO, characterized by a connectivity mostly involving oral sensorimotor and gustatory areas/subcortical structures. The present data suggest, based on connectivity patterns, an involvement of area GrFO in the cortical circuits for controlling goal-directed hand and face/mouth actions. In this context, area GrFO could represent a gateway for the access of limbic inputs, for example about subjective values, emotional significance of stimuli or internal states, to the PMv areas involved in selecting appropriate goal-directed hand and mouth/face actions.


Hand motor control Limbic system Gustatory cortex Premotor cortex 



The work was supported by Ministero dell’Istruzione, dell’Università e della Ricerca (grant number: PRIN 2010, 2010MEFNF7_005), European Commission Grant Cogsystems FP7-250013, and Interuniversity Attraction Poles (IAP) P7/11.


  1. Amaral D, Behniea H, Kelly J (2003) Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 118:1099–1120CrossRefPubMedGoogle Scholar
  2. Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244CrossRefPubMedGoogle Scholar
  3. Barbas H (2007) Specialized elements of orbitofrontal cortex in primates. Ann NY Acad Sci 1121:10–32CrossRefPubMedGoogle Scholar
  4. Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256:211–228CrossRefPubMedGoogle Scholar
  5. Belmalih A, Borra E, Contini M, Gerbella M, Rozzi S, Luppino G (2009) Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex. J Comp Neurol 512:183–217CrossRefPubMedGoogle Scholar
  6. 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 728:724Google Scholar
  7. Borra E, Gerbella M, Rozzi S, Luppino G (2011) Anatomical evidence for the involvement of the macaque ventrolateral prefrontal area 12r in controlling goal-directed actions. J Neurosci 31:12351–12363CrossRefPubMedGoogle Scholar
  8. Brass M, Haggard P (2010) The hidden side of intentional action: the role of the anterior insular cortex. Brain Struct Funct 214:603–610CrossRefPubMedGoogle Scholar
  9. Caggiano V, Fogassi L, Rizzolatti G, Casile A, Giese MA, Thier P (2012) Mirror neurons encode the subjective value of an observed action. Proc Natl Acad Sci USA 109:11848–11853PubMedCentralCrossRefPubMedGoogle Scholar
  10. Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366–402CrossRefPubMedGoogle Scholar
  11. Carmichael ST, Price JL (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642–664CrossRefPubMedGoogle Scholar
  12. Chudasama Y, Daniels TE, Gorrin DP, Rhodes SE, Rudebeck PH, Murray EA (2013) The role of the anterior cingulate cortex in choices based on reward value and reward contingency. Cereb Cortex 23:2884–2898PubMedCentralCrossRefPubMedGoogle Scholar
  13. Cipolloni PB, Pandya DN (1999) Cortical connections of the frontoparietal opercular areas in the rhesus monkey. J Comp Neurol 403:431–458CrossRefPubMedGoogle Scholar
  14. Devinsky O I, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306CrossRefGoogle Scholar
  15. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in primate cerebral cortex. Cereb Cortex 1:1–47CrossRefPubMedGoogle Scholar
  16. Ferrari PF, Gallese V, Rizzolatti G, Fogassi L (2003) Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci 17:1703–1714CrossRefPubMedGoogle Scholar
  17. Ferrari PF, Rozzi S, Fogassi L (2005) Mirror neurons responding to observation of actions made with tools in monkey ventral premotor cortex. J Cogn Neurosci 17:212–226CrossRefPubMedGoogle Scholar
  18. Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS (2004) Receptive field properties of the macaque second somatosensory cortex: evidence for multiple functional representations. J Neurosci 24:11193–11204PubMedCentralCrossRefPubMedGoogle Scholar
  19. Fluet MC, Baumann MA, Scherberger H (2010) Context-specific grasp movement representation in macaque ventral premotor cortex. J Neurosci 30:15175–15184CrossRefPubMedGoogle Scholar
  20. Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organization of inferior area 6 in the macaque monkey: I. Somatotopy and the control of proximal movements. Exp Brain Res 71:475–490CrossRefPubMedGoogle Scholar
  21. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2010) Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. Cereb Cortex 20:141–168CrossRefPubMedGoogle Scholar
  22. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2011) Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Struct Funct 216:43–65CrossRefPubMedGoogle Scholar
  23. Gerbella M, Borra E, Rozzi S, Tonelli S, Luppino G (2012) Cortical connections of architectonically distinct areas of the Macaque frontal operculum. In: Federation of European Neurosciences Societies Abstr Program No. 2806Google Scholar
  24. Gerbella M, Borra E, Tonelli S, Rozzi S, Luppino G (2013) Connectional heterogeneity of the ventral part of the macaque area 46. Cereb Cortex 23:967–987CrossRefPubMedGoogle Scholar
  25. Grabenhorst F, Rolls ET (2011) Value, pleasure and choice in the ventral prefrontal cortex. Trends Cogn Sci 15:56–67CrossRefPubMedGoogle Scholar
  26. Hayden BY, Platt ML (2010) Neurons in anterior cingulate cortex multiplex information about reward and action. J Neurosci 30:3339–3346PubMedCentralCrossRefPubMedGoogle Scholar
  27. Huang CS, Hiraba H, Murray GM, Sessle BJ (1989) Topographical distribution and functional properties of cortically induced rhythmical jaw movements in the monkey (Macaca fascicularis). J Neurophysiol 61:635–650PubMedGoogle Scholar
  28. Ibañez A, Gleichgerrcht E, Manes F (2010) Clinical effects of insular damage in humans. Brain Struct Funct 214:397–410CrossRefPubMedGoogle Scholar
  29. Jones EG, Burton H (1976) Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates. J Comp Neurol 168:197–248CrossRefPubMedGoogle Scholar
  30. Jürgens U, Ehrenreich L (2007) The descending motorcortical pathway to the laryngeal motoneurons in the squirrel monkey. Brain Res 1148:90–95CrossRefPubMedGoogle Scholar
  31. Krubitzer L, Clarey J, Tweedale R, Elston G, Calford M (1995) A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J Neurosci 15:3821–3839PubMedGoogle Scholar
  32. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534CrossRefPubMedGoogle Scholar
  33. Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G (1991) Multiple representations of body movements in mesial area 6 and the adjacent cingulated cortex: an intracortical microstimulation study in the macaque monkey. J Comp Neurol 311:463–482CrossRefPubMedGoogle Scholar
  34. 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 17:559–578CrossRefPubMedGoogle Scholar
  35. Maranesi M, Rodà F, Bonini L, Rozzi S, Ferrari PF, Fogassi L, Coudé G (2012) Anatomo-functional organization of the ventral primary motor and premotor cortex in the macaque monkey. Eur J Neurosci 36:3376–3387CrossRefPubMedGoogle Scholar
  36. Martin RE, Sessle BJ (1993) The role of the cerebral cortex in swallowing. Dysphagia 8:195–202CrossRefPubMedGoogle Scholar
  37. Martin RE, Kemppainen P, Masuda Y, Yao D, Murray GM, Sessle BJ (1999) Features of cortically evoked swallowing in the awake primate (Macaca fascicularis). J Neurophysiol 82:1529–1541PubMedGoogle Scholar
  38. Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of macaque monkey. Behav Brain Res 18:125–137CrossRefPubMedGoogle Scholar
  39. Matelli M, Luppino G, Fogassi L, Rizzolatti G (1989) Thalamic input to inferior area 6 and area 4 in the macaque monkey. J Comp Neurol 280:468–488CrossRefPubMedGoogle Scholar
  40. Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and of the adjacent cingulate cortex. J Comp Neurol 311:445–462CrossRefPubMedGoogle Scholar
  41. 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 402:327–352CrossRefPubMedGoogle Scholar
  42. Matsuzaka Y, Aizawa H, Tanji J (1992) A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. J Neurophysiol 68:653–662PubMedGoogle Scholar
  43. Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J Comp Neurol 212:1–22CrossRefPubMedGoogle Scholar
  44. Nelissen K, Vanduffel W (2011) Grasping-related functional magnetic resonance imaging brain responses in the macaque monkey. J Neurosci 31:8220–8229PubMedCentralCrossRefPubMedGoogle Scholar
  45. Ogawa H (1994) Gustatory cortex of primates: anatomy and physiology. Neurosci Res 20:1–13CrossRefPubMedGoogle Scholar
  46. Ogawa H, Ito S, Nomura T (1989) Oral cavity representation at the frontal operculum of macaque monkeys. Neurosci Res 6:283–298CrossRefPubMedGoogle Scholar
  47. Olszewski J (1952) The thalamus of Macaca Mulatta. S. Karger, New YorkGoogle Scholar
  48. Padoa-Schioppa C, Cai X (2011) The orbitofrontal cortex and the computation of subjective value: consolidated concepts and new perspectives. Ann N Y Acad Sci 1239:130–137PubMedCentralCrossRefPubMedGoogle Scholar
  49. Pardo-Vazquez JL, Leboran V, Acuna C (2008) Neural correlates of decisions and their outcomes in the ventral premotor cortex. J Neurosci 28:12396–12408CrossRefPubMedGoogle Scholar
  50. Pritchard TC, Hamilton RB, Morse JR, Norgren R (1986) Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J Comp Neurol 244:213–228CrossRefPubMedGoogle Scholar
  51. Roberts T, Akert K (1963) Insular and opercular cortex and its thalamic projections in Macaca mulatta. Sweiz Archiv Neurol Neurochir Psychiatr 92:1–43Google Scholar
  52. 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 16:1389–1417CrossRefPubMedGoogle Scholar
  53. Russchen FT, Amaral DG, Price JL (1987) The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey Macaca fascicularis. J Comp Neurol 256:175–210CrossRefPubMedGoogle Scholar
  54. Saleem KS, Miller B, Price JL (2014) Subdivisions and connectional networks of the lateral prefrontal cortex in the macaque monkey. J Comp Neurol 522:1641–1690CrossRefPubMedGoogle Scholar
  55. Schell G, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539–560PubMedGoogle Scholar
  56. Shima K, Tanji J (1998) Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282:1335–1338CrossRefPubMedGoogle Scholar
  57. Simonyan K, Jürgens U (2002) Cortico-cortical projections of the motorcortical larynx area in the rhesus monkey. Brain Res 949:23–31CrossRefPubMedGoogle Scholar
  58. Simonyan K, Jürgens U (2003) Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey. Brain Res 974:43–45CrossRefPubMedGoogle Scholar
  59. Simonyan K, Jürgens U (2005a) Afferent cortical connections of the motor cortical larynx area in the rhesus monkey. Neuroscience 130:133–149CrossRefPubMedGoogle Scholar
  60. Simonyan K, Jürgens U (2005b) Afferent subcortical connections into the motor cortical larynx area in the rhesus monkey. Neuroscience 130:119–131CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Marzio Gerbella
    • 1
    • 2
  • Elena Borra
    • 1
  • Stefano Rozzi
    • 1
  • Giuseppe Luppino
    • 1
  1. 1.Dipartimento di Neuroscienze, Sezione di FisiologiaUniversità di ParmaParmaItaly
  2. 2.Brain Center for Social and Motor CognitionIstituto Italiano di Tecnologia (IIT)ParmaItaly

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