Summary
The functional properties of neurons located in the rostral part of inferior area 6 were studied in awake, partially restrained macaque monkeys. The most interesting property of these neurons was that their firing correlated with specific goal-related motor acts rather than with single movements made by the animal. Using the motor acts as the classification criterion we subdivided the neurons into six classes, four related to distal motor acts and two related to proximal motor acts. The distal classes are: “Grasping-with-the-hand-and-the-mouth neurons”, “Grasping-with-the-hand neurons”, “Holding neurons” and “Tearing neurons”. The proximal classes are: “Reaching neurons” and “Bringing-to-the-mouth-or-to-the-body neurons”. The vast majority of the cells belonged to the distal classes. A particularly interesting aspect of distal class neurons was that the discharge of many of them depended on the way in which the hand was shaped during the motor act. Three main groups of neurons were distinguished: “Precision grip neurons”, “Finger prehension neurons”, “Whole hand prehension neurons”. Almost the totality of neurons fired during motor acts performed with either hand. About 50% of the recorded neurons responded to somatosensory stimuli and about 20% to visual stimuli. Visual neurons were more difficult to trigger than the corresponding neurons located in the caudal part of inferior area 6 (area F4). They required motivationally meaningful stimuli and for some of them the size of the stimulus was also critical. In the case of distal neurons there was a relationship between the type of prehension coded by the cells and the size of the stimulus effective in triggering the neurons. It is proposed that the different classes of neurons form a vocabulary of motor acts and that this vocabulary can be accessed by somatosensory and visual stimuli.
Similar content being viewed by others
References
Brinkman C, Porter R (1979) Supplementary motor area in the monkey: activity of neurons during performance of a learned motor task. J Neurophysiol 42: 681–709
Buys EJ, Lemon RN, Mantel GWH, Muir RB (1986) Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J Physiol (Lond) 381: 529–549
Cowey A (1979) Cortical maps and visual perception. Q J Exp Psychol 31: 1–17
Evarts EV (1984) Hierarchies and emergent features in motor control. In: Edelman G, Gall W, Cowan W (eds) Dynamic aspects of neocortical functions. Wiley, New York, pp 557–579
Evarts EV, Shinoda Y, Wise SP (1984) Neurophysiological approaches to higher brain functions. Wiley, New York, 193 p
Fetz EE, Cheney PD (1980) Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol 44: 751–772
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 control of proximal movements. Exp Brain Res 71: 475–490
Godschalk M, Lemon RN, Nijs HOT, 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: 113–116
Haaxma R, Kuypers HGJM (1975) Intrahemispheric cortical connections and visual guidance of hand and finger movements in the rhesus monkey. Brain 98: 239–260
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 51–112
Kaas JK (1983) What, if anything, is SI? Organization of first somatosensory area of cortex. Physiol Rev 63: 206–231
Kurata K, Okano K, Tanji J (1985) Distribution of neurons related to hindlimb as opposed to forelimb movement in the monkey premotor cortex. Exp Brain Res 60: 188–191
Kurata K, Tanji J (1986) Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci 6: 403–411
Leinonen L, Nyman G (1979) II. Functional properties of cells in anterolateral part of area 7 associative face area of awake monkey. Exp Brain Res 34: 321–333
Leinonen L, Hyvärinen J, Nyman G, Linnankoski I (1979) I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys. Exp Brain Res 34: 299–320
Lemon RN, Mantel GWH, Muir RB (1986) Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. J Physiol (Lond) 381: 497–527
Martino AM, Strick PL (1987) Corticospinal projections originate from the arcuate premotor area. Brain Res 404: 307–312
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: 125–137
Moll L, Kuypers HGJM (1977) Premotor cortical ablations in monkeys: contralateral changes in visually guided behavior. Science 198: 317–319
Muir RB, Lemon RN (1983) Corticospinal neurons with a special role in precision grip. Brain Res 261: 312–316
Neff WD, Diamond IT, Casseday JH (1975) Behavioral studies of auditory discrimination: central nervous system. In: Keidel WD, Neff WD (eds) Auditory system. Handbook of sensory physiology, Vol 5, Part 2. Springer, Berlin Heidelberg New York, pp 307–400
Okano K, Tanji J (1987) Neuronal activities in the primate motor fields of the agranular frontal cortex preceding visually triggered and self-placed movement. Exp Brain Res 66: 155–166
Penfield W, Jasper H (1954) Epilepsy and the functional anatomy of the human brain. Little Brown, Boston, Mass., 100 p
Penfield W, Welch K (1951) Supplementary motor area of the cerebral cortex. Arch Neurol Psychiat 66: 289–317
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
Rizzolatti G, Gentilucci M (1988) Motor and visual-motor functions of the premotor cortex. In: Rakic P, Singer W (eds) Neurobilogy of Neocortex. Dahlem Konferenzen. Wiley, New York, pp 269–284
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: 421–424
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: 125–146
Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981c) Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2: 147–163
Rizzolatti G, Gentilucci M, Fogassi L, Luppino G, Matelli M, Ponzoni Maggi S (1987) Neurons related to goal-directed motor acts in inferior area 6 of the macaque monkey. Exp Brain Res 67: 220–224
Rosenbaum DA (1980) Human movement initiation: specification of arm, direction, and extent. J Exp Psychol [Gen] 109: 444–474
Rosenquist AC (1985) Connections of visual cortical areas in the cat. In: Peters A, Jones EG (eds) Cerebral cortex, Vol 3, Plenum Press, New York, pp 81–117
Shinoda Y, Yokota JI, Futami T (1981) Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey. Neurosci Lett 23: 7–12
Tanji J (1984) The neuronal activity in the supplementary motor area of primates. Trends Neurosci 7: 282–285
Van Essen DC, Maunsell JHR (1983) Hierarchical organization and functional streams in the visual cortex. Trends Neurosci 6: 370–375
Weinrich M, Wise SP (1982) The premotor cortex of the monkey. J Neurosci 2: 1329–1345
Wiesendanger M (1981) Organization of secondary motor areas of cerebral cortex. In: Brooks VB (ed) Nervous system, Vol II, Motor control, Part 2. Handbook of physiology. American Physiological Society, Bethesda, Md., pp 1121–1148
Wiesendanger M, Seguin JS, Künzle H (1973) The supplementary motor area — a control system for posture? In: Stein RB, Pearson KC, Smith RS, Redford JB (eds) Control of posture and locomotion. Plenum Press, New York, pp 331–346
Wise SP (1985) The primate premotor cortex: past, present and preparatory. Annu Rev Neurosci 8: 1–19
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: 238–264
Zeki SM (1982) The mapping of visual functions in the cerebral cortex. In: Katsuki Y, Norgren R, Sato M (eds) Brain mechanisms of sensation. Wiley, New York, pp 105–128
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rizzolatti, G., Camarda, R., Fogassi, L. et al. Functional organization of inferior area 6 in the macaque monkey. Exp Brain Res 71, 491–507 (1988). https://doi.org/10.1007/BF00248742
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00248742