Maurizio Gentilucci

Functional organization of inferior area 6 in the macaque monkey

SummaryTwo 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.

Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses

The visual response of single neurons of the periarcuate cortex have been studied in the macaque monkey. Two sets of neurons responding to visual stimuli have been found. The first set, located rostral to the arcuate sulcus, was formed by units that could be activated by stimuli presented far from the animal. These neurons had large receptive fields and were neither orientation nor direction selective. The second set, found predominantly caudal to the arcuate sulcus, was formed by units that were maximally or even exclusively activated by stimuli presented in the space immediately around the animal. These neurons were bimodal, responding also to somatosensory stimuli. According to the location of their visual responding regions the bimodal neurons were subdivided into pericutaneous (54%) and distant peripersonal neurons (46%). The former responded best to stimuli presented a few centimeters from the skin, the latter to stimuli within the animals reaching distance. The visual responding regions were spatially related to the tactile fields. It is argued that neurons with a receptive field consisting of several responding areas, some in one sensory modality, some in another, have a praxic function and that they are involved in organizing sequences of movements.

Visual illusion and action

The role of allocentric cues on movement control was investigated in the present study. Pointing movements directed to the more distant vertex of closed and open configurations of the Muller-Lyer illusion, as well as to the vertex of control lines, were studied in four experimental conditions. In the first (full-vision condition) subjects saw both stimulus and their hand before and during movement, in the second (non-visual feedback condition) they saw the stimulus, but not their hand during movement. In the two remaining conditions (no-vision conditions) vision of the scene and the hand was precluded. Pointing was executed 0 sec (no vision 0 sec delay condition) or 5 sec (no-vision 5 sec delay condition) after the light was switched off. The Muller-Lyer illusion affected pointing kinematics with respect to the control lines. Subjects undershot and overshot the vertex location, respectively, of the closed and open configuration. Correspondingly, the entire kinematics were changed. The main result was, however, a gradually increasing effect of the perceptual illusion when pointing was executed from memory compared to the full-vision condition. These data are discussed according to the hypothesis that the system underlying visual perception in the allocentric frame of reference and that involved in motor action can functionally interact. The strength of this interaction depends upon the efficiency of the egocentric frame of reference by which motor actions are constructed.

Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position

SummaryThe visual responses of postarcuate neurons have been studied in alert behaving monkeys (Macaca nemestrina). In particular, the effect of eye position on the location of visual responses in respect to the body has been examined. It was found that a large percentage of bimodal (visual and somatosensory) neurons have visual receptive fields that are independent of eye position. The location of the visual receptive field does not change when the eyes move, but remains in register with the tactile receptive field (soma-related visually responsive neurons).

Space coding by premotor cortex

SummaryMany neurons in inferior area 6, a cortical premotor area, respond to visual stimuli presented in the space around the animal. We were interested to learn whether the receptive fields of these neurons are coded in retinotopic or in body-centered coordinates. To this purpose we recorded single neurons from inferior area 6 (F4 sector) in a monkey trained to fixate a light and detect its dimming. During fixation visual stimuli were moved towards the monkey both within and outside the neuronss receptive field. The fixation point was then moved and the neuron retested with the monkeys gaze deviated to the new location. The results showed that most inferior area 6 visual neurons code the stimulus position in spatial and not in retinal coordinates. It is proposed that these visual neurons are involved in generating the stable body-centered frame of reference necesary for programming visually guided movements.

Neurons related to reaching-grasping arm movements in the rostral part of area 6 (area 6aβ)

SummarySingle neurons were recorded from the rostral part of the agranular frontal cortex (area 6aβ) in awake, partially restrained macaque monkeys. In the medialmost and mesial sectors of this area, rostral to the supplementary motor area, neurons were found which were activated during arm reaching-grasping movements. These neurons (“reaching-grasping neurons”) did not appear to be influenced by how the objects were grasped nor, with some exceptions, by where they were located. Their activity changed largely prior to the arm movement and continued until the end of it. The premovement modulation (excitatory or inhibitory) could start with stimulus presentation, with the saccade triggered by the stimulus or after stimulus fixation. The distance of the stimulus from the monkey was an important variable for activating many neurons. About half of the recorded neurons showed a modulation of the same sign during movement and premovement period. The other half showed an increase/decrease in activity which was of the opposite sign during movement and premovement period or part of it. In this last case the discharge changes were of the same sign when the stimulus was close to the monkey and when the monkey moved its arm to reach the objects, whereas they were of opposite sign when the stimulus was outside the animals reach. Microstimulation of area 6aβ and the reconstruction of the locations of eye movement and arm movement related cells showed that the arm field was located more medially (and mesially) than the eye field described by Schlag and Schlag-Rey (1987). It is suggested that, unlike inferior area 6, which is mostly involved in selection of effectors on the basis of the physical properties of the objects and their spatial location (Rizzolatti and Gentilucci 1988), area 6aβ plays a role in the preparation of reaching-grasping arm movements and in their release when the appropriate conditions are set.

Speech and gesture share the same communication system

Humans speak and produce symbolic gestures. Do these two forms of communication interact, and how? First, we tested whether the two communication signals influenced each other when emitted simultaneously. Participants either pronounced words, or executed symbolic gestures, or emitted the two communication signals simultaneously. Relative to the unimodal conditions, multimodal voice spectra were enhanced by gestures, whereas multimodal gesture parameters were reduced by words. In other words, gesture reinforced word, whereas word inhibited gesture. In contrast, aimless arm movements and pseudo-words had no comparable effects. Next, we tested whether observing word pronunciation during gesture execution affected verbal responses in the same way as emitting the two signals. Participants responded verbally to either spoken words, or to gestures, or to the simultaneous presentation of the two signals. We observed the same reinforcement in the voice spectra as during simultaneous emission. These results suggest that spoken word and symbolic gesture are coded as single signal by a unique communication system. This signal represents the intention to engage a closer interaction with a hypothetical interlocutor and it may have a meaning different from when word and gesture are encoded singly.

Coordination between the transport and the grasp components during prehension movements

In this study, the possible influence of the transport on the grasp component of prehension movements was investigated. The first phase of the transport (acceleration phase) and of the grasp (finger aperture phase) kinematics were studied under conditions of visual and non-visual object presentation (prehension experiment). In the non-visual condition, object size was estimated by haptics and object position was estimated by proprioception. Eight subjects were required to reach and grasp three objects of different size located at two distances. An additional experiment (matching experiment) was carried out to control the scaling of object size in the two conditions. The results showed that in the matching experiment size estimation for large objects was similar in the two conditions, whereas small stimuli were underestimated in the haptic condition. In the prehension experiment, maximal finger aperture and velocity of finger aperture were greater in the non-visual than in the visual condition, and the difference was greater for small than for large stimuli. Moreover, in both conditions, finger opening was larger for prehension movements directed to the far than to the near objects, but only for smaller stimuli. Hand trajectory variability increased in the non-visual condition and with the distance, whereas finger opening variability was only affected by the non-visual condition. For smaller stimuli, increased finger opening with distance was positively correlated with the increase in wrist variability in the visual condition, but not in the non-visual condition. Furthermore, increased finger opening between visual and non-visual conditions was correlated with the increase in wrist variability, for smaller objects at the near object location. No positive correlations were found between finger opening and grip variability. These results are interpreted in favour of the dependence of finger opening on transport, when control requirements during reaching increase.

The role of proprioception in the control of prehension movements: a kinematic study in a peripherally deafferented patient and in normal subjects.

In this study we investigated the role of proprioception in the control of prehension movements, with particular reference to the grasp component. Grasp and transport kinematics were studied in a peripherally deafferented patient and in five healthy subjects. Two experiments were carried out: the prehension experiment and the grasp perturbation experiment. In the prehension experiment both the patient and the control subjects were required to reach and grasp three objects of different size, located at three different distances, both with and without visual feedback. In the grasp perturbation experiment a mechanical perturbation was applied to the fingers during prehension movements, again executed with and without visual feedback. In the prehension experiment temporal parameters of the patients movements were generally slowed, with greater variability on some measures. However, over the first phase of the movement the pattern of the patients hand opening and transport acceleration, scaled to object size and distance, was the same as that of controls, both with and without visual feedback. On the contrary, during the final phase of the movement (the finger closure phase and deceleration) the patients performance differed significantly from the controls. These phases were abnormally lengthened and frequent movement adjustments were observed. In the grasp perturbation experiment the patient was not able to compensate for the perturbations applied to the fingers, even with visual feedback. The data allowed us to investigate also the respective contribution of proprioception and of vision of the hand in the control of prehension. We compared prehension kinematics in two conditions: (a) with visual but no proprioceptive feedback (in the patient) and (b) with proprioceptive but no visual feedback (in the controls). In both experiments proprioceptive control was more efficient than visual control. The results of this study are interpreted in favour of the strict dependence of prehension control on proprioception. The first phase of the movement, however, can be appropriately planned and executed without the necessity of either proprioceptive or visual information about the hand.

Temporal coupling between transport and grasp components during prehension movements: effects of visual perturbation

The temporal coupling between the transport and grasp components of prehension movements was investigated through two experiments. In Experiment 1, six normal subjects were required to reach and grasp each of three spheres located at three different distances (Blocked trials). In Experiment 2, a visual perturbation paradigm was used in which the location of the object to be reached and grasped could change at the beginning of arm movement (Perturbed trials). The same subjects participated in both experiments. Kinematics of wrist trajectory (transport component) and of distance between thumb and index finger (grasp component) were analyzed. The results of Experiment 1 showed that the two components could be temporally coupled during their time course. In Experiment 2, the visual perturbation affected both the components, but different times were required by each component to reorganize the movement towards the new target. These different times caused the decoupling of those events that appeared synchronized in Experiment 1. Finally, evidence was found to suggest that planning of grip formation takes into account not only the perceived characteristics of the object, but also the time planned by the transport component to reach the object.