Experimental Brain Research

, Volume 71, Issue 3, pp 475–490 | Cite as

Functional organization of inferior area 6 in the macaque monkey

I. Somatotopy and the control of proximal movements
  • M. Gentilucci
  • L. Fogassi
  • G. Luppino
  • M. Matelli
  • R. Camarda
  • G. Rizzolatti


Two series of experiments are reported in this paper. The first concerns the movement representation in the macaque inferior area 6, the second the functional properties of neurons located in the caudal part of this area (histochemical area F4). By combining single neuron recording and intracortical microstimulation, we found that inferior area 6 is somatotopically organized. The axio-proximal movements are represented caudally, the distal movements are represented near the arcuate sulcus. The mouth field is located laterally, the hand field medially. There is no leg field. A comparison between neuron properties and histochemical characteristics of inferior area 6 showed that the proximal movements representation includes most of area F4, whereas the distal movements representation corresponds to area F5 and to the rostral part of F4. Neurons located in that part of F4 where proximal movements are represented respond very well to tactile stimuli. They have large receptive fields mostly located on the face and on the upper part of the body. A large number of these neurons respond to visual stimuli. Objects approaching the animal are particularly effective. The tactile and the visual receptive fields are in register. The most represented movements are reaching movements, movements bringing the hand to the mouth or to the body and facial movements. There is a congruence between location of visual fields and preferred arm movements. It is argued that the receptive field arrangement and the response properties are more complex in area F4 than in the primary motor cortex and that area F4 neurons are involved in the control of arm movements towards different space sectors.

Key words

Area 6 Macaque monkey Somatotopic map Proximal movements Visually responsive neurons 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alstermark B, Lundberg A, Norrsell U, Sybirska E (1981) Integration in descending motor pathways controlling the forelimb in the cat. 9. Differential behavioural defects after spinal cord lesions interrupting defined pathways from higher centres to motoneurones. Exp Brain Res 42: 299–318Google Scholar
  2. Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the Rhesus monkey. J Comp Neurol 256: 211–228Google Scholar
  3. Fulton JF (1934) Forced grasping and grasping in relation to the syndrome of the premotor area. Arch Neurol Psychiat 31: 221–235Google Scholar
  4. Gentilucci M, Scandolara C, Pigarev IN, Rizzolatti G (1983) Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position. Exp Brain Res 50: 464–468Google Scholar
  5. Godschalk M, Lemon RN, Nijs HGT, Kuypers HGJM (1981) Behaviour of neurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements. Exp Brain Res 44: 113–116Google Scholar
  6. Godschalk M, Lemon RN, Kuypers HGJM, Ronday HK (1984) Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study. Exp Brain Res 56: 410–424Google Scholar
  7. Halsband U, Passingham R (1982) The role of premotor and parietal cortex in the direction of action. Brain Res 240: 368–372Google Scholar
  8. Humphrey DR (1979) On the cortical control of visually directed reaching: contributions by nonprecentral motor areas. In: Talbot RE, Humphrey DR (eds) Posture and movement. Raven Press, New York, pp 51–112Google Scholar
  9. Hyvärinen J (1982) The parietal cortex of monkey and man. Studies of brain function, Vol 8. Springer, Berlin Heidelberg New York, 202 pGoogle Scholar
  10. Illert M, Lundberg A, Tanaka R (1976) Integration in descending motor pathways controlling the forelimb in the cat. 1. Pyramidal effects on motoneurons. Exp Brain Res 26: 509–519Google Scholar
  11. Illert M, Lundberg A, Tanaka R (1977) Integration in descending motor pathways controlling the forelimb in the cat. 3. Convergence on propriospinal neurones transmitting disynaptic excitation from the corticospinal tract and other descending tracts. Exp Brain Res 29: 323–346Google Scholar
  12. Künzle H (1978) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrental regions (area 6 and 9) in Macaca fascicularis. Brain Behav Evol 15: 185–234Google Scholar
  13. Kurata K, Tanji J (1986) Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci 6: 403–411Google Scholar
  14. Kwan HC, MacKay WA, Murphy JT, Wong YC (1978) Spatial organization of precentral cortex in awake primates. II. Motor outputs. J Neurophysiol 41: 1120–1131Google Scholar
  15. Lemon RN, Porter R (1976) Afferent input to movement-related precentral neurones in conscious monkeys. Proc R Soc Lond [Biol] 194: 313–339Google Scholar
  16. Lemon RN, Hanby JA, Porter R (1976) Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys. Proc R Soc Lond [Biol] 194: 341–373Google Scholar
  17. Lynch JC (1980) The functional organization of posterior parietal association cortex. Behav Brain Sci 3: 485–534Google Scholar
  18. Martino AM, Strick PL (1987) Corticospinal projections originate from the arcuate premotor area. Brain Res 404: 307–312Google Scholar
  19. Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res 18: 125–137Google Scholar
  20. Matelli M, Camarda R, Glickstein M, Rizzolatti G (1986) Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol 251: 281–298Google Scholar
  21. Matsumura M, Kubota K (1979) Cortical projection of hand-arm motor area from postarcuate area in macaque monkey: a histological study of retrograde transport of horseradish peroxidase. Neurosci Lett 11: 241–246Google Scholar
  22. Moll L, Kuypers HGJM (1977) Premotor cortical ablation in monkeys: contralateral changes in visually guided reaching behavior. Science 198: 317–319Google Scholar
  23. 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: 871–908Google Scholar
  24. Muakkassa KF, Strick PL (1979) Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized “premotor” areas. Brain Res 177: 176–182Google Scholar
  25. Murray EA, Coulter GD (1981) Organization of cortico-spinal neurons in the monkey. J Comp Neurol 195: 339–365Google Scholar
  26. Penfield W, Welch K (1951) Supplementary motor area of the cerebral cortex. Arch Neurol Psychiat 66: 289–317Google Scholar
  27. Petrides M (1982) Motor conditional associative-learning after selective prefrontal lesions in the monkey. Behav Brain Res 5: 407–413Google Scholar
  28. Phillips GC, Porter R (1977) Corticospinal neurones. Their role in movement. Academic Press, London, 450 pGoogle Scholar
  29. Pigarev IN, Rodionova EI (1986) Neurons with visual receptive fields independent of eye position in the caudal part of the ventral bank of cat cruciate sulcus. Neurophysiology (Kiev) 18: 800–804Google Scholar
  30. Rizzolatti G, Scandolara C, Gentilucci M, Camarda R (1981a) Response properties and behavioral modulation of “mouth” neurons of the postarcuate cortex (area 6) in macaque monkeys. Brain Res 255: 421–424Google Scholar
  31. Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981b) Afferent properties of periarcuate neurons in macaque monkeys. I. Somato-sensory responses. Behav Brain Res 2: 125–146Google Scholar
  32. Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981c) Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2: 147–163Google Scholar
  33. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res 71: 491–507Google Scholar
  34. Sessle BJ, Wiesendanger M (1982) Structural and functional definition of the motor cortex in the monkey (Macaca fascicularis). J Physiol (Lond) 323: 245–265Google Scholar
  35. Strick PL (1985) How do the basal ganglia and cerebellum gain access to the cortical motor areas? Behav Brain Res 18: 107–123Google Scholar
  36. Toyoshima K, Sakai H (1982) Exact cortical extent of the origin of the corticospinal tract (CST) and the quantitative contribution to the CST in different cytoarchitectonic areas. A study with horseradish peroxidase in the monkey. J Hirnforsch 23: 257–269Google Scholar
  37. Wannier TMJ, Tollte M, Hepp-Reymond MC (1986) On the problem of multiple hand representation in area 4 of the alert Macaca fascicularis. Experientia 42: 711Google Scholar
  38. Weinrich M, Wise SP (1982) The premotor cortex of the monkey. J Neurosci 2: 1329–1345Google Scholar
  39. Weinrich M, Wise SP, Mauritz KH (1984) A neurophysiological study of the premotor cortex in the Rhesus monkey. Brain 107: 385–414Google Scholar
  40. Wise SP (1985) The primate premotor cortex: past, present and preparatory. Annu Rev Neurosci 8: 1–19Google Scholar
  41. Wong YC, Kwan HC, MacKay WA, Murphy JT (1978) Spatial organization of precentral cortex in awake primates. I. Somatosensory inputs. J Neurophysiol 41: 1107–1119Google Scholar
  42. Woolsey CN, Settlage PH, Meyer DR, Sencer W, Pinto Hamuy T, Travis AM (1952) Patterns of localization in precentral and “supplementary” motor areas and their relation to the concept of a premotor area. Res Publ Assoc Nerv Ment Dis 30: 238–264Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • M. Gentilucci
    • 1
  • L. Fogassi
    • 1
  • G. Luppino
    • 1
  • M. Matelli
    • 1
  • R. Camarda
    • 1
  • G. Rizzolatti
    • 1
  1. 1.Istituto di Fisiologia UmanaUniversitá di ParmaParmaItaly

Personalised recommendations