[Motor thalamus connections with area 4 and 6 in the monkey].
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Biomedical subjects
Publications and source records attributed to G Rizzolatti.
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The rostral part of the agranular frontal cortex (area 6) can be subdivided on the basis of its cytoarchitecture, enzymatic properties, and connections into two large sectors: a superior region, lying medial to the spur of the arcuate sulcus, and an inferior region, lying lateral to it. In this study we traced the afferent and efferent connections of the inferior region of area 6 by injecting small amounts of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) and fluorescent tracers (fast blue and diamidino yellow) into restricted parts of inferior area 6 and in physiologically determined fields of area 4. There is an ordered topographic pattern of connections between inferior area 6 and area 4. The region near the spur of the arcuate sulcus (hand field) projects to the area 4 hand field while the lateral part of inferior area 6 (mouth field) is connected with the corresponding field in area 4. The organization of the connections between the two fields is, however, different. The hand fields in area 6 and 4 have direct reciprocal projections, whereas the mouth field in the postarcuate cortex relays information to area 4 via a zone intermediate between the arcuate and the central sulcus. This zone corresponds to the cytochrome oxidase area F4 (Matelli, Luppino, and Rizzolatti: Behav. Brain Res. 18: 125-137, '85). The inferior area 6 also has topographically organized connections with the supplementary motor area. The inferior area 6 receives and sends fibers to a series of discrete cortical areas located in the lower cortical moiety (Sanides: The Structure and Function of the Nervous Tissue, Vol. 5. New York: Academic Press, pp 329-453, '72). These areas that form a broad ring around the central sulcus are the ventral bank of the principal sulcus and the adjacent area 46, the precentral operculum (PrOC), area SII (Jones and Burton: J. Comp. Neurol. 168:197-248, '76), the parietal operculum, and the rostral part of the inferior parietal lobule including the lower bank of the intraparietal sulcus. Finally, the inferior area 6 has sparse but consistent connections with insular and cingulate cortices. The functional significance of this complex pattern of connections is discussed.
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The study was aimed at testing various models that can explain visual lateral asymmetries due to hemispheric specialization. In Experiments 1-3 the subjects had to perform a lateralized "go-no go" discrimination of words (primary task) either alone or in association with secondary tasks that interfered with the processing of the left hemisphere (ordered tapping) or the right hemisphere (finger flexion). In Experiment 4 the primary task was one of lateralized "go-no go" discrimination of faces while the secondary tasks were again those of ordered tapping and finger flexion. The results showed that in the case of word discrimination the advantage in speed of response in favour of the right visual field/left hemisphere (RVF/LH), which was observed for the primary task alone, did not change when the secondary task was added. This held true irrespective of whether the secondary task loaded the left or right hemisphere. The advantage for the left visual field/right hemisphere (LVF/RH) observed for face discrimination alone, disappeared when the secondary task interfered with the processing of the right hemisphere and did not change when the secondary task concerned the left hemisphere. It was concluded that each hemisphere is able to elaborate in parallel the incoming information, but, in normal conditions, interhemispheric transmission is responsible for the lateral asymmetries in perception (conditional interhemispheric transmission model).
Small amounts of horseradish peroxidase conjugated with wheat germ were injected in restricted parts of the postarcuate premotor area of the macaque monkey. It was found that regions of this area having different somatotopic representations are richly interconnected among them. This pattern of intra-areal connectivity was not observed in the precentral motor area. It appears therefore that the postarcuate area is organized according to anatomical principles which are different from those of the primary motor cortex.
Horseradish peroxidase conjugated with wheat germ agglutinine was injected in restricted parts of the postarcuate cortex in the macaque monkey. Anterograde and retrograde transport was found in the parietal and frontal lobes. In the parietal lobe two areas were marked: the antero-lateral part of area 7 and the superior bank of the sylvian fissure. In the frontal lobe the marked areas were the precentral motor cortex, the supplementary motor area and the gyrus cinguli. The intrinsic connections within the postarcuate cortex were rich and widespread. The hand representation was connected anterogradely and retrogradely with the mouth representation and anterogradely with the leg representation; the mouth representation was connected both ways with the hand representation but not with the leg area. The richness of intrinsic connections in the postarcuate cortex supports the suggestion that this area is involved in the organization of sequential motor acts.
Single neurons and polispike activity were recorded from the superior colliculus of anesthetized, behaving monkeys. In agreement with previous findings neurons of the superficial layers responded exclusively to visual stimuli. In the intermediate layers most neurons were oculomotor, although some of them showed also a visual receptive field. No neurons responding to tactile or auditory stimuli were found. Occasionally the discharge of an oculomotor neuron increased if the ocular movement was triggered by a visual or an acoustical stimulus. Rare tacticle and auditory neurons were recorded in deep layers. However their receptive fields were difficult to map and their responses lacked the precision of the responses of the specific acoustic and tactile areas. Electrical stimulation of the SC produced contralateral eye and head movements, the threshold being high in the superficial layers and low in the intermediate and deep ones. In the deep layers complex limb and trunk movements could be also elicited. In conclusion, in contrast with carnivores and other mammals, the primate superior colliculus appears to be dominated by the visual modality.
The effect of unilateral surgical ablations of lateral part of inferior parietal lobule (area 7b) has been studied in the macaque monkey. The following neurological deficits were found: 1) A hemi-inattention for tactile stimuli applied to the hemiface and hand contralateral to the lesion; 2) A hemi-inattention for visual stimuli in the contralateral peripersonal space; 3) A reluctance to use the contralateral arm; 4) A mild and transient deficit in mouth grasping movements towards stimuli contralaterally presented; 5) Postural abnormalities of the hand contralateral to the lesion. It is proposed that area 7b is involved in the perception of the peripersonal space and in the organization of movements towards stimuli presented in that space.
Simple reaction times to lateralized visual stimuli were studied in normal subjects while they were carrying out a concomitant task. The concomitant task consisted in the exploration of a visual maze presented in the middle of a screen. Regardless of the hand used, the concomitant task produced a specific lengthening of the responses to stimuli located in the left visual field. It is concluded that the right hemisphere plays a major role in the organization of ocular movements during active exploration of visual environment.
Two experiments are described in which simple reaction times (RTs) to lateralized visual stimuli were measured in normal subjects during negative affect and during recollection of everyday life scenes. In both experiments the mental activity produced a remarkable increase of RTs with respect to a control situation without interfering activity. During production of the negative affect there was a selective lengthening of RTs mediated by the right hemisphere. The role of the right hemisphere in producing emotions is discussed.
The 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).
The neurological deficits following section of the midbrain commissures were studied in the cat. After a lesion of the commissures between the superior and inferior colliculi, with or without involvement of the posterior commissure, the animals showed a long lasting inattention for stimuli in the upper visual space, lack of exploratory head movements towards the neglected space, head ventroflexion and vertical paralysis of gaze. After a lesion of the commissure between the superior colliculi or of its rostral part only, the same symptomatology appeared, but it was short lasting. After a lesion of the posterior commissure, the head was kept dorsiflexed, the exploratory head movements towards the lower visual space were reduced and the stimuli presented in this space were often neglected. There was a paralysis of vertical eye movements. The findings are discussed in the frame of a premotor theory of neglect.
The effect of unilateral surgical ablations of the postarcuate cortex (area 6) has been studied in the macaque monkey (Macaca irus). Two series of neurological deficits were found: (1) a failure to grasp food with the mouth when presented contralaterally to the lesion and a reluctance to use the contralateral hand; (2) a severe hemi-inattention. This was present in both the somatosensory and visual modalities but, in the latter, was limited to the peripersonal space. Both motor and attentional deficits improved with time. However, when the symptomatology was stabilized, the animals tended to use the ipsilateral hand and, when presented with two stimuli, preferred that ipsilateral to the lesion. Control experiments in which area 8 (frontal eye fields) was ablated unilaterally showed a decrease of eye movements contralateral to the lesion and a neglect of the contralateral hemispace. No somatosensory deficits were found. The visual neglect was more prominent for 'far' space than for that near the animal. The role of area 6 in organizing motor acts and the strict relation between the type of motor deficit and the type of neglect are discussed.
Simple reaction times to lateralized unstructured visual stimuli were measured in normal subjects while they were carrying out concomitant left hemisphere tasks. Three tasks were used. In the first task the subjects had to pay attention to strings of digits, acoustically presented, and detect letters randomly interspersed among the digits; in the second task the subjects had to memorize strings of acoustically presented digits; in the third task they had to repeat each digit of a string as soon as they heard it. In spite of the greater difficulty of the first two tasks with respect to the third one, only this last task, the only one requiring a verbo-motor response, produced a significant disadvantage for the left hemisphere responses to light. It is argued that in RT experiments a specific left hemisphere interference takes place when the secondary task requires the organization of a motor response
Stimulus-response compatibility effects have been hypothesized to result (a) from a subject's innate tendency to respond in the direction of the source of stimulation, (b) from a correspondence between the spatial codes associated with the effector and the stimulus, or (c) from an attentional bias favoring the effector located in the same hemispace as the command signal. Two experiments were conducted to test these three hypotheses. In Experiment 1 the subjects were requested to make unimanual discriminative key-pressing responses to two light stimuli, both appearing to either the right or left of the fixation point. In one condition the two hands were in anatomical position (uncrossed); in the other they were crossed. The procedure of Experiment 2 was similar to that of Experiment 1 with the exception that both hands, always in an uncrossed position, were placed on the same side of the body midline (on the right or left). The results showed that the compatibility effect depends on a correspondence between the spatial codes associated with the location of the effector and the location of the command stimulus.
Subpial unilateral ablations of the postarcuate cortex (area 6) were performed in four macaque monkeys. After the operation the animals showed a tactile contralateral neglect and a visual neglect for stimuli presented in the space immediately around the contralateral hemiface, they tended to use the hand ipsilateral to the lesion and their mouth and face movements in response to contralateral stimuli were disorganized. No primary motor deficits were described. With time there was a marked recovery of the symptomatology, but the preference for using the ipsilateral hand and extinction of the contralateral stimuli were present until the animals' death. The deficits after the postarcuate cortex are discussed with reference to previous electrophysiological data.