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G Luppino

Publications and source records attributed to G Luppino.

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Space coding by premotor cortex.

Many 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 neuron's receptive field. The fixation point was then moved and the neuron retested with the monkey's 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 necessary for programming visually guided movements.

Animals

Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey.

The agranular frontal cortex is formed by several distinct functional areas. There is no agreement, however, on its cytoarchitectonic organization. The aim of this study was to redefine the cytoarchitectonic organization of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. A particular goal was to find out whether the so-called supplementary motor area (SMA) is cytoarchitectonically different from the rest of area 6 and whether it can be considered as a single, independent cytoarchitectonic area. The results showed that, rostral to F1 (area 4), four architectonic areas can be recognized in the superior (dorsal) and mesial area 6. Two fo them are located on mesial cortical surface (F3 caudally and F6 rostrally) and two on superior cortical convexity (F2 caudally and F7 rostrally). The main cytoarchitectonic features of the five identified areas can be summarized as follows. F1: (1) giant pyramidal cells organized in multiple rows, (2) columnar pattern extending from the white matter to the superficial layers, (3) low cellular density in the lower part of layer III. F3: (1) high cellular density in the lower part of layer III, which fuses with a dense Va, (2) columnar pattern present only in the deepest layer, (3) occasional presence of giant pyramidal cells in layer Vb. F6: (1) prominent layer V, (2) absence of sublayer Vb, (3) homogeneous cell density in superficial layers. F2: (1) thin row of medium-size pyramids in the lowest part of layer III, (2) columnar pattern extending to the superficial layers, (3) dense layer Va, (4) few, scattered giant pyramids in layer Vb. F7: (1) prominent layer V, (2) bipartite layer VI. Areas F1, F2, and F3, as defined cytoarchitectonically, coincided with the homonymous histochemical areas. The present data showed also that area 24 is formed by four subareas: 24a, b, c and d. Areas 24a and b occupy the ventral part of area 24, whereas its dorsal part is formed by area 24c, located rostrally, and area 24d, located caudally. The following features distinguish area 24d from area 24c: (1) larger pyramidal cells in layer V, (2) presence of medium-size pyramidal cells in the lower part of layer III, (3) more prominent columnar pattern, (4) higher myelinization with the presence of an evident horizontal plexus. Mesial area 6 is usually considered as a single functional entity (SMA). Our findings show that this cortical region is formed by two distinct cytoarchitectonic areas.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey.

The mesial agranular frontal cortex that lies rostral to area 4 (F1) is formed by two distinct cytoarchitectonic areas: F3, located caudally, and F6, located rostrally. In the present experiments we investigated the organization of F3 and F6 by observing the motor responses evoked by their intracortical electrical microstimulation. Our main purpose was to find out whether the cytoarchitectonic subdivision of the mesial agranular frontal cortex into two areas has a physiological counterpart. The result showed that F3 (the caudal area) contains a complete motor representation with hindlimb movements located caudally, forelimb movements located centrally, and orofacial movements located rostrally. The great majority of limb movements involved proximal joints. With respect to F1, F3 showed the following functional characteristics: (1) lack of segregation between proximal and distal movements, (2) larger percentage of complex movements, and (3) higher excitability threshold. Movements were more difficult to elicit from F6 (the rostral area) than from F3. However, by using a longer stimulus train duration (100 ms) 39.3% of tested sites produced body movements. This percentage increased (50.5%) when the electrical stimulation was applied during monkey natural movements instead of when the monkey was still in its chair. Most of the evoked movements concerned the forelimb. More rarely, neck and upper face movements were observed. Unlike F1 and F3 where most movements were fast, slow movements were frequently observed with stimulation of F6. Many of them mimicked natural movements of the animal. Eye movements were evoked from F7 (superior area 6) but not from F6. An additional motor representation was found in the dorsocaudal part of area 24 (24d). This area is topographically organized with a forelimb representation located caudally and ventrally and a hindlimb representation located rostrally and dorsally. The excitability threshold of area 24d is higher than that of F1 and F3. Evoked movements were occasionally observed also after stimulation of area 24c. In conclusion, on the mesial cortical wall rostral to F1, there are at least three independent motor representations. On the basis of somatotopic organization and excitability properties, we propose that the term supplementary motor area (SMA-proper) should be reserved to F3.

Animals

Cortico-cortical connections of two electrophysiologically identified arm representations in the mesial agranular frontal cortex.

Neuronal tracers (diamidino yellow or wheat germ agglutinin conjugated with horseradish peroxidase) were injected in the arm representations of area 6a alpha (mesial surface, area F3), in the arm representation of area 6a beta (mesial surface) as well as in the eye field of area 6a beta (dorso-medial surface). The results showed that the arm representation of area F3 receives topographically organized afferents from motor and premotor areas (areas F1, F2, F4 and F5). A further connection was found with that part of cingulate cortex that sends projections to the spinal cord. In contrast, the arm representation of area 6a beta receives afferents chiefly from area F5, the prefrontal cortex and that part of cingulate sulcus which has few, if any, connections with the spinal cord. No connections were found with the precentral motor cortex (area F1). The area 6a beta eye field receives afferents mostly from the frontal eye field. Further connections are with the prefrontal cortex and cingulate gyrus. It is suggested that the so called "low level" motor functions of supplementary motor area are due to the activity of area F3, whereas the so called "high level" motor functions depend upon an independent area located in area 6a beta.

Animals

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

Single neurons were recorded from the rostral part of the agranular frontal cortex (area 6a beta) 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 animal's reach. Microstimulation of area 6a beta 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 6a beta plays a role in the preparation of reaching-grasping arm movements and in their release when the appropriate conditions are set.

Animals

Thalamic input to inferior area 6 and area 4 in the macaque monkey.

Recent cytoarchitectonic, histochemical, and hodological studies in primates have shown that area 6 is formed by three main sectors: the supplementary motor area, superior area 6, which lies medial to the spur of the arcuate sulcus, and inferior area 6, which is located lateral to it. Inferior area 6 has been further subdivided into two histochemical areas: area F5, located along the inferior limb of the arcuate sulcus, and area F4, located between area F5 and area 4 (area F1). The present study traced the thalamocortical projections of inferior area 6 and the adjacent part of area 4 by injecting small amounts of WGA-HRP in specific sectors of the agranular frontal cortex. Our data showed that each histochemical area receives a large projection from one nucleus of the ventrolateral thalamus (motor thalamus) and additional projections from other nuclei of this thalamic sector. Area F5 receives a large projection from area X of Olszewski ('52) and additional projections from the caudal part of the nucleus ventralis posterior lateralis, pars oralis (VPLo), and the nucleus ventralis lateralis, pars caudalis (VLc) (VPLo-VLc complex). Area F4 receives a large projection from the nucleus ventralis lateralis, pars oralis (VLo), and additional projections from area X and the VPLo-VLc complex. The rostral part of area F1 is innervated chiefly by VLo, plus smaller contributions from rostral VPLo and the VPLo-VLc complex. The caudal part of F1 receives its greatest input from VPLo, with a small contribution from VLo. In addition, each histochemical area receives projections originating from the intralaminar thalamic nuclei, the posterior thalamus, and--for area F4 and area F5--also from the nucleus medialis dorsalis (MD). Analysis of the physiological properties of the various histochemical areas in relation to their main thalamic input showed that those cortical fields in which distal movements are predominant (area F5, caudal part of area F1) are innervated chiefly by area X and VPLo, whereas those cortical fields in which proximal movements are predominant receive their main input from VLo. Because VPLo and area X are targets of cerebellothalamic pathways, whereas VLo receives a pallidal input, we propose that the cortical fields in which distal movements are most heavily represented are mainly under the influence of the cerebellum, whereas the cortical fields in which proximal movements are most heavily represented are mainly under the influence of the basal ganglia.

Animals

Somatotopic representation in inferior area 6 of the macaque monkey.

On the basis of its cytoarchitectonic and enzymatic properties area 6 of the macaque monkey can be subdivided into two large sectors: a superior sector lying medial to the spur of the arcuate sulcus (superior area 6 or F2) and an inferior sector lying lateral to it (inferior area 6). Inferior area 6 is constituted by two enzymatic areas: F4 and F5. In this study we investigated the somatotopic organization of inferior area 6 and the adjacent area 4 combining single-neuron recording and intracortical electrical microstimulation. We found that two separate movement representations exist in this region. The caudal one corresponds to area F1 (primary motor cortex), the rostral one to inferior area 6. The two representations are mirror images one of the other with the axioproximal movements being adjacently located. In the rostral map the proximal movements are mostly located in F4, the distal movements in F5. Neuronal properties indicate that the rostral map has characteristics that are more complex than the caudal map. We propose that the rostral map is involved in transforming visual information in motor commands. F4 should be involved in the control of arm movements based on the location of the objects in respect to the body, whereas F5 should play a role in the control of grasping movements on the basis of the size of the stimuli.

Animals

New view of the organization of the pulvinar nucleus in Tupaia as revealed by tectopulvinar and pulvinar-cortical projections.

The projections of the superficial layers of the superior colliculus to the pulvinar nucleus in Tupaia were reexamined by injecting WGA-HRP into the tectum. The main result was finding two different patterns of terminations in the pulvinar nucleus: a zone remote from the lateral geniculate nucleus, which occupies the dorsomedial and caudal poles of the pulvinar nucleus, was almost entirely filled with terminals in every case irrespective of the location of the injection site; and a second division of the pulvinar nucleus, adjacent to the lateral geniculate nucleus, contained irregular patches--much more densely populated--and the distribution of patches varied from case to case. We call the first projection "diffuse" and the patchy projection "specific." Next we injected several divisions of the extrastriate visual cortex to find the cortical target of each pathway. The diffuse path terminates in the ventral temporal area (Tv). The specific path terminates in the dorsal temporal area (Td) and area 18. We speculated about the significance of the two pathways: the specific path may be responsible for the preservation of vision after removal of the striate cortex; the diffuse path may have an important place in the evolution of the visual areas of the temporal and occipital lobe. We argued that the target of the diffuse path is in a position to relate limbic and visual impulses and relay the product of such integration to the other visual areas, striate as well as extrastriate cortex.

Animals

Cholinergic projections from the midbrain reticular formation and the parabigeminal nucleus to the lateral geniculate nucleus in the tree shrew.

The distribution and sources of putative cholinergic fibers within the lateral geniculate nucleus (GL) of the tree shrew have been examined by using the immunocytochemical localization of choline acetyltransferase (ChAT). ChAT-immunoreactive fibers are found throughout the thalamus but are particularly abundant in the GL as compared to other principal sensory thalamic nuclei (medial geniculate nucleus, ventral posterior nucleus). Individual ChAT-immunoreactive fibers are extremely fine in caliber and display numerous small swellings along their lengths. Within the GL, ChAT-immunoreactive fibers are more numerous in the layers than in the interlaminar zones and, in most cases, the greatest density is found in layers 4 and 5. Two sources for the ChAT-immunoreactive fibers in the GL have been identified--the parabigeminal nucleus (Pbg) and the pedunculopontine tegmental nucleus (PPT)--and the contribution that each makes to the distribution of ChAT-immunoreactive fibers in GL was determined by combining immunocytochemical, axonal transport, and lesion methods. The projection from the Pbg is strictly contralateral, travels via the optic tract, and terminates in layers 1, 3, 5, and 6 as well as the interlaminar zones on either side of layer 5. The projection from PPT is bilateral (ipsilateral dominant) and terminates throughout the GL as well as in other thalamic nuclei. Lesions of the Pbg eliminate the ChAT-immunoreactive fibers normally found in the optic tract but have no obvious effect on the density of ChAT-immunoreactive fibers in the contralateral GL. In contrast, lesions of PPT produce a conspicuous decrease in the number of ChAT-immunoreactive fibers in the GL and in other thalamic nuclei on the side of the lesion but have no obvious effect on the number of ChAT-immunoreactive fibers in the optic tract. These results suggest that there are two sources of cholinergic projections to the GL in the tree shrew which are likely to play different roles in modulating the transmission of visual activity to the cortex. The Pbg is recognized as a part of the visual system by virtue of its reciprocal connections with the superficial layers of the superior colliculus, while the PPT is a part of the midbrain reticular formation and is thought to play a non-modality-specific role in modulating the activity of neurons throughout the thalamus and in other regions of the brainstem.

Animals

Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements.

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.

Animals

Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements.

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 assessed by somatosensory and visual stimuli.

Animals

Neurons related to goal-directed motor acts in inferior area 6 of the macaque monkey.

A new class of neurons was identified in the rostral part of inferior area 6 in the macaque monkey (Macaca nemestrina). These neurons fire in relation to motor acts which have a particular aim such as reaching, grasping or holding. The same neuron discharges when the animal uses the right hand, the left hand and, frequently, also the mouth. Furthermore most of these neurons specify how the aim can be achieved (e.g. precision grip vs whole hand prehension). Different types of goal-related neurons form a vocabulary of simple motor acts localized in inferior area 6.

Action Potentials

Evidence of interhemispheric transmission in laterality effects.

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).

Cerebral Cortex

Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey.

The laminar pattern of cytochrome oxidase activity was studied in the agranular frontal cortex (area 4-6 complex) of the macaque monkey. The cortex, stained with this method, showed 6 stripes of different enzymatic activity. On the basis of their characteristics and of the presence of highly active cells, the agranular frontal cortex could be parcellated in 5 areas (F1-F5). F1 very likely corresponds to area FA of von Bonin and Bailey. Rostral to F1 two large regions could be distinguished, one located medial to the spur of the arcuate sulcus and its imaginary caudal extension, the other laterally. The superior region was formed by areas F2 and F3. The first was located on the dorsomedial cortical surface, the other on the mesial surface. F3 possibly corresponds to the supplementary motor area. The inferior region was formed by areas F4 and F5. The rostral area (F5) showed transition characteristics that rendered it somehow similar to the prefrontal areas. It may correspond to the cytoarchitectonic area FCBm. The cytocrome oxidase technique is a useful means of parcellating the agranular frontal cortex and may greatly help in physiological and behavioral experiments.

Animals