The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity

Springer Science and Business Media LLC - Tập 89 - Trang 571-580 - 1992
L. Bon1, C. Lucchetti1
1Istituto di Fisiologia, Universita' di Trieste, Trieste, Italy

Tóm tắt

The activity of 249 neurons in the dorsomedial frontal cortex was studied in two macaque monkeys. The animals were trained to release a bar when a visual stimulus changed color in order to receive reward. An acoustic cue signaled the start of a series of trials to the animal, which was then free to begin each trial at will. The monkeys tended to fixate the visual stimuli and to make saccades when the stimuli moved. The monkeys were neither rewarded for making proper eye movements nor punished for making extraneous ones. We found neurons whose discharge was related to various movements including those of the eye, neck, and arm. In this report, we describe the properties of neurons that showed activity related to visual fixation and saccadic eye movement. Fixation neurons discharged during active fixation with the eye in a given position in the orbit, but did not discharge when the eye occupied the same orbital positions during nonactive fixation. These neurons showed neither a classic nor a complex visual receptive field, nor a foveal receptive visual field. Electrical stimulation at the site of the fixation neurons often drove the eye to the orbital position associated with maximal activity of the cell. Several different kinds of neurons were found to discharge before saccades: 1) checking-saccade neurons, which discharged when the monkeys made self-generated saccades to extinguish LED's; 2) novelty-detection saccade neurons, which discharged before the first saccade made to a new visual target but whose activity waned with successive presentations of the same target. These results suggest that the dorsomedial frontal cortex is involved in attentive fixation. We hypothesize that the fixation neurons may be involved in codifying the saccade toward a target. We propose that their involvement in arm-eye-head motor-planning rests primarily in targeting the goal of the movement. The fact that saccaderelated neurons discharge when the saccades are self initiated, implies that this area of the cortex may share the control of voluntary saccades with the frontal eye fields and that the activation is involved in intentional motor processes.

Tài liệu tham khảo

Berlucchi G, Moruzzi G, Salvi G, Strata P (1964) Pupil behavior and ocular movements during synchronized and desynchronized sleep. Arch Ital Biol 102: 230–244 Bizzi E (1968) Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp Brain Res 6: 69–80 Bon L, Corazza R, Inchingolo P (1980) Eye movements during the waking-sleep cycle of the encephale isole' semichronic cat preparation. Electroencephalogr Clin Neurophysiol 48: 327–340 Bon L, Lucchetti N (1990) Neurons signalling the maintenance of attentive fixation in frontal area 6aβ of macaque monkey. Exp Brain Res 82: 231–233 Bon L, Lucchetti N (1991) Behavioral and motor mechanisms of dorsomedial frontal cortex of macaca monkey. Int J Neurosci (in press) Brodmann K (1905) Beiträge zur histologischen Lokalisation der Grosshirnrinde: die Rindenfelder der niederen Affen. J Psychol Neurol 4:177–226 Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603–635 Evarts EV (1968) A technique for recording activity of subcortical neurons in moving animal. Electroencephalogr Clin Neurophysiol 24: 83–86 Godschalk M, Lemon RN (1983) Involvement of monkey premotor cortex in the preparation of arm movement. Exp Brain Res [Suppl] 7: 114–119 Godschalk M, Lemon RN, Kuypers HGJM, Van der Steen J (1985) The involvement of monkey premotor cortex neurons in preparation of visually cued arm movement. Behav Brain Res 18: 143–157 Goldberg ME, Bruce CJ (1990) Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. J Neurophysiol 64: 489–508 Goldman-Rakic PS (1988) Topography of cognition: parallel distributed networks in primate association cortex. Ann Rev Neurosci 11: 137–56 Guitton D, Buchtel HA, Douglas RM (1982) Disturbances of voluntary saccadic eye movement mechanisms following discrete unilateral frontal lobe removals. In: Functional basis of ocular motility disorders. Lennerstrand G, Zee DS, Keller EL (eds) Pergamon Press, Oxford, pp 497–500 Halsband U, Passingham R (1982) The role of premotor and parietal cortex in the direction of action. Brain Res 244: 368–372 Huerta MF, Kaas JH (1990) Supplementary eye field as defined by intracortical microstimulation: connections in macaques. J Comp Neurol 293: 299–330 Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coil for measurement of eye position: an improved method. Vis Res 20: 535–538 Kubota K, Hamada I (1978) Visual tracking and neuron activity in the post arcuate area in monkeys. J Physiol Paris 74: 297–312 Kurata K, Wise SP (1988) Premotor and supplementary motor cortex in rhesus monkeys: neuronal activity during externallyand internally-instructed motor tasks. Exp Brain Res 72: 237–248 Mann SE, Thau R, Schiller PH (1988) Conditional task-related responses in monkey dorsomedial frontal cortex. Exp Brain Res 69: 460–468 Mott FW, Schaefer EA (1890) On associated eye-movements produced by cortical faradization of the monkey's brain. Brain 13: 165–173 Mountcastle VB, Andersen RA, Motter AN (1981) The influence of attentive fixation upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J Neurosci 1: 1218–1234 Posner MI, Petersen SE (1990) The attention system of the human brain. Ann Rev Neurosci 13: 25–42 Posner MI, Rothbart MK (1991) Attentional mechanisms and conscious experience. In the neuropsychology of consciousness (eds) Milner AD, Rugg MD, Academic Press (in press) Remmel RS (1984) An inexpensive eye movement monitor using the sciera coil technique. IEEE Trans Biomed Engin, BME 31, 4: 388–390 Rizzolatti G, Gentilucci M, Camarda R, Gallese V, Luppino G, Matelli M, Fogassi L (1990) Neurons related to reaching grasping arm movements in rostral part of area 6 (area 6αβ) Exp Brain Res 82: 337–350 Rizzolatti G, Matelli M, Pavesi G (1983) Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106: 655–673 Schlag J, Schlag-Rey M (1987a) Evidence for a supplementary eye field. J Neurophysiol 57: 179–200 Schlag J, Schlag-Rey M (1987b) Does microstimulation evoke fixed-vector saccades by generating their vector of by specifying their goal? Exp Brain Res 68: 442–444 Shook BL, Schlag-Rey M, Schlag J (1990) Primate supplementary eye field. I. Comparative aspects of mesencephalic and pontine connections. J Comp Neurol 301: 618–642 Shook BL, Schlag-Rey M, Schlag J (1991) Primate supplementary eye field. II. Comparative aspects of connections with the thalamus, corpus striatum, and related forebrain nuclei. J Comp Neurol 307: 562–583 Suzuki H, Azuma M (1977) Prefrontal neuronal activity during gazing at a light spot in the monkey. Brain Res 126: 497–508 Voght O, Voght N (1919) Ergebnisse unserer Hirnforschung. J Psychol Neurol (Leipzig) 25: 277–462 Von Bonin G, Bailey P (1947) The neocortex of macaca mulatta. University of Illinois Press, Urbana Weinrich M, Wise SP (1982) The premotor cortex of the monkey. J Neurosci 2: 1329–1345 Weinrich M, Wise SP, Moritz KH (1984) A neurophysiological analysis of the premotor cortex of the monkey. Brain 107: 385–414 Wise SP, Mauritz KH (1985) Set-related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set. Proc R Soc Lond A 223: 331–354