Claudio Galletti

Superior Area 6 Afferents From the Superior Parietal Lobule in the Macaque Monkey

Superior area 6 of the macaque monkey frontal cortex is formed by two cytoarchitectonic areas: F2 and F7. In the present experiment, we studied the input from the superior parietal lobule (SPL) to these areas by injecting retrograde neural tracers into restricted parts of F2 and F7. Additional injections of retrograde tracers were made into the spinal cord to define the origin of corticospinal projections from the SPL. The results are as follows: 1) The part of F2 located around the superior precentral dimple (F2 dimple region) receives its main input from areas PEc and PEip (PE intraparietal, the rostral part of area PEa of Pandya and Seltzer, [1982] J. Comp. Neurol. 204:196–210). Area PEip was defined as that part of area PEa that is the source of corticospinal projections. 2) The ventrorostral part of F2 is the target of strong projections from the medial intraparietal area (area MIP) and from the dorsal part of the anterior wall of the parietooccipital sulcus (area V6A). 3) The ventral and caudal parts of F7 receive their main parietal input from the cytoarchitectonic area PGm of the SPL and from the posterior cingulate cortex. 4) The dorsorostral part of F7, which is also known as the supplementary eye field, is not a target of the SPL, but it receives mostly afferents from the inferior parietal lobule and from the temporal cortex. It is concluded that at least three separate parietofrontal circuits link the superior parietal lobule with the superior area 6. Considering the functional properties of the areas that form these circuits, it is proposed that the PEc/PEip‐F2 dimple region circuit is involved in controlling movements on the basis of somatosensory information, which is the traditional role proposed for the whole dorsal premotor cortex. The two remaining circuits appear to be involved in different aspects of visuomotor transformations. J. Comp. Neurol. 402:327–352, 1998.

Parietal neurons encoding spatial locations in craniotopic coordinates

The receptive fields of visual neurons are known to be retinotopically arranged, and in awake animals they “move” with gaze, maintaining the same retinotopic location regardless of eye position. Here, we report the existence in the monkey parietal cortex of cells (called “real-position” cells) whose receptive field does not systematically move with gaze. These cells respond to the visual stimulation of the same spatial location regardless of eye position and therefore directly encode visual space in craniotopic instead of retinotopic coordinates.

Functional Magnetic Resonance Imaging Reveals the Neural Substrates of Arm Transport and Grip Formation in Reach-to-Grasp Actions in Humans

Picking up a cup requires transporting the arm to the cup (transport component) and preshaping the hand appropriately to grasp the handle (grip component). Here, we used functional magnetic resonance imaging to examine the human neural substrates of the transport component and its relationship with the grip component. Participants were shown three-dimensional objects placed either at a near location, adjacent to the hand, or at a far location, within reach but not adjacent to the hand. Participants performed three tasks at each location as follows: (1) touching the object with the knuckles of the right hand; (2) grasping the object with the right hand; or (3) passively viewing the object. The transport component was manipulated by positioning the object in the far versus the near location. The grip component was manipulated by asking participants to grasp the object versus touching it. For the first time, we have identified the neural substrates of the transport component, which include the superior parieto-occipital cortex and the rostral superior parietal lobule. Consistent with past studies, we found specialization for the grip component in bilateral anterior intraparietal sulcus and left ventral premotor cortex; now, however, we also find activity for the grasp even when no transport is involved. In addition to finding areas specialized for the transport and grip components in parietal cortex, we found an integration of the two components in dorsal premotor cortex and supplementary motor areas, two regions that may be important for the coordination of reach and grasp.

Brain location and visual topography of cortical area V6A in the macaque monkey

The brain location, extent and functional organization of the cortical visual area V6A was investigated in macaque monkeys by using single cell recording techniques in awake, behaving animals. Six hemispheres of four animals were studied. Area V6A occupies a horseshoe‐like region of cortex in the caudalmost part of the superior parietal lobule. It extends from the medial surface of the brain, through the anterior bank of the parieto‐occipital sulcus, up to the most lateral part of the fundus of the same sulcus. Area V6A borders on areas V6 ventrally, PEc dorsally, PGm medially and MIP laterally. Of 1348 neurons recorded in V6A, 61% were visual and 39% non‐visual in nature. The visual neurons were particularly sensitive to orientation and direction of movement of visual stimuli. The inferior contralateral quadrant was the most represented one. Visual receptive fields were also found in the inferior ipsilateral quadrant and in the upper visual field. Receptive fields were on average smaller in the lower visual field than in the upper one. Both central and peripheral parts of the visual field were represented. Large parts of the visual field were represented in small regions of area V6A, and the same regions of the visual field were re‐represented many times in different parts of this area, without any apparent topographical order. The only reliable sign of retinotopic organization was the predominance of central representation dorsally and far periphery ventrally. The functional organization of area V6A is discussed in the view that this area could be involved in the control of reaching out and grasping objects.

Wide-Field Retinotopy Defines Human Cortical Visual Area V6

The retinotopic organization of a newly identified visual area near the midline in the dorsalmost part of the human parieto-occipital sulcus was mapped using high-field functional magnetic resonance imaging, cortical surface-based analysis, and wide-field retinotopic stimulation. This area was found in all 34 subjects that were mapped. It represents the contralateral visual hemifield in both hemispheres of all subjects, with upper fields located anterior and medial to areas V2/V3, and lower fields medial and slightly anterior to areas V3/V3A. It contains a representation of the center of gaze distinct from V3A, a large representation of the visual periphery, and a mirror-image representation of the visual field. Based on similarity in position, visuotopic organization, and relationship with the neighboring extrastriate visual areas, we suggest it might be the human homolog of macaque area V6, and perhaps of area M (medial) or DM (dorsomedial) of New World primates.

Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey

We have compared physiological data recorded from three alert macaque monkeys with separate observations of local connectivity, to locate and characterize the functional border between two related but distinct visual areas on the caudal face of the superior parietal gyrus. We refer to these areas as V6 and V6A. They occupy almost the entire extent of the anterior bank of the parieto‐occipital sulcus, V6A being the more dorsal. These two areas are strongly interconnected. Anatomically, we have defined the border as the point at which labelled axon terminals first adopt a recognizably ‘descending’ pattern in their laminar characteristics, after injections of wheatgerm agglutinin‐horseradish peroxidase into the dorsal half of the gyrus (in presumptive V6A). A similar principle was used to recognize the same border by the pattern of input from area V5, except that in this case the relevant transition in laminar characteristics is that between an ‘intermediate’ pattern (in V6) and an ‘ascending’ pattern (in V6A). V6A was found to be distinct from V6 in a number of its physiological properties. Unlike V6, it contains visually unresponsive cells as well as units with craniotopic receptive fields (‘real‐position’ cells), units tuned to very slow stimulus speeds, units with complex visual selectivities and units with activity related to attention. V6A was also found to have a larger mean receptive field size and scatter than V6. By contrast, response properties related to the basic orientation and direction of moving bar stimuli were indistinguishable between V6 and V6A, as was the influence of gaze direction on cell activity in the two areas. Two‐dimensional maps of the recording sites allowed reconstruction of the V6/V6A border. For comparison, the anatomical results were rendered on two‐dimensional maps of identical format to those used to summarize the physiological data. After normalizing for relative size, the physiological and connectional estimates of the border between V6 and V6A were found to coincide, at least within the range of individual variation between hemispheres. An architectonic map in the same format was also made from a hemisphere stained for myelin and Nissl substance. Area PO, defined by its general density of myelination was not distinct in this material, but several architectural features were traceable and one of these was also found to approximate the V6/V6A border. The particular criteria that distinguish V6 from V6A differ from a recent description of areas PO and POd in the Cebus monkey; we believe it most likely that PO and POd together may correspond to V6.

The cortical connections of area V6: an occipito-parietal network processing visual information

The aim of this work was to study the cortical connections of area V6 by injecting neuronal tracers into different retinotopic representations of this area. To this purpose, we first functionally recognized V6 by recording from neurons of the parieto‐occipital cortex in awake macaque monkeys. Penetrations with recording syringes were performed in the behaving animals in order to inject tracers exactly at the recording sites. The tracers were injected into the central or peripheral field representation of V6 in different hemispheres. Irrespective of whether injections were made in the centre or periphery, area V6 showed reciprocal connections with areas V1, V2, V3, V3A, V4T, the middle temporal area /V5 (MT/V5), the medial superior temporal area (MST), the medial intraparietal area (MIP), the ventral intraparietal area (VIP), the ventral part of the lateral intraparietal area and the ventral part of area V6A (V6AV). No labelled cells or terminals were found in the inferior temporal, mesial and frontal cortices. The connections of V6 with V1, and with all the retinotopically organized prestriate areas, were organized retinotopically. The connection of V6 with MIP suggests a visuotopic organization for this latter. Labelling in V6A and VIP after either central or peripheral V6 injections was very similar in location and extent, as expected on the basis of the nonretinotopic organization of these areas. We suggest that V6 plays a pivotal role in the dorsal visual stream, by distributing the visual information coming from the occipital lobe to the sensorimotor areas of the parietal cortex. Given the functional characteristics of the cells of this network, we suggest that it could perform the fast form and motion analyses needed for the visual guiding of arm movements as well as their coordination with the eyes and the head.

The cortical visual area V6: brain location and visual topography

The brain location and topographical organization of the cortical visual area V6 was studied in five hemispheres of four awake macaque monkeys. Area V6 is located in the caudal aspect of the superior parietal lobule (SPL). It occupies a ‘C’‐shaped belt of cortex whose upper branch is in the depth of the parieto‐occipital sulcus (POS) and lower one is in the depth of the medial parieto‐occipital sulcus (POM), with the medial surface of the brain as a zone of junction between the two branches. Area V6 contains a topographically organized representation of the contralateral visual field up to an eccentricity of at least 80 °. The lower visual field representation is located dorsally, in the ventral part of POS, and the upper field ventrally, in the dorsal wall of POM. The representation of the horizontal meridian forms the posterior border of V6. It is adjacent to area V3 in POS as well as in the caudal part of POM, on the ventral convexity of the brain. The lower vertical meridian forms the anterior border of V6, adjacent to area V6A. The upper vertical meridian is in the depth of POM. The representation of the central visual field is not magnified relative to that of the periphery. The central visual field (below 20–30 ° of eccentricity) is represented in the medial‐most aspect of the annectant gyrus, in the lateral part of the posterior bank of POS. The visuotopic organization of area V6 suggests a role in the analysis of the flow field resulting from self‐motion, in selecting targets during visual searching as well as in the control of arm‐reaching movements towards non‐foveated targets.

Arm Movement-related Neurons in the Visual Area V6A of the Macaque Superior Parietal Lobule

Area V6A is a cortical visual area located in the posterior face of the superior parietal lobule in the macaque monkey. It contains visual neurons as well as neurons not activated by any kind of visual stimulation. The aim of this study was to look for possible features able to activate these latter neurons. We tested 70 non‐visual V6A neurons. Forty‐three of them showed an arm movement–related neural discharge due to somatosensory stimulation and/or skeletomotor activity of the upper limbs of the animal. The arm movement‐related neural discharge started before the onset of arm movement, often before the earliest lectromyographic activity. Thus, although the discharge is probably supported by proprioceptive and tactile inputs it is not fully dependent on them. Arm movement‐related neurons of area V6A seem to be well equipped for integrating motor signals related to arm movements with somatosensory signals evoked by those ovements. Taking into account also the visual characteristics of V6A neurons, it seems likely that area V6A as a whole is involved in the visual guiding of reaching

The Dorsomedial Pathway Is Not Just for Reaching: Grasping Neurons in the Medial Parieto-Occipital Cortex of the Macaque Monkey

Brain control of prehension is thought to rely on two specific brain circuits: a dorsomedial one (involving the areas of the superior parietal lobule and the dorsal premotor cortex) involved in the transport of the hand toward the object and a dorsolateral one (involving the inferior parietal lobule and the ventral premotor cortex) dealing with the preshaping of the hand according to the features of the object. The present study aimed at testing whether a pivotal component of the dorsomedial pathway (area V6A) is involved also in hand preshaping and grip formation to grasp objects of different shapes. Two macaque monkeys were trained to reach and grasp different objects. For each object, animals used a different grip: whole-hand prehension, finger prehension, hook grip, primitive precision grip, and advanced precision grip. Almost half of 235 neurons recorded from V6A displayed selectivity for a grip or a group of grips. Several experimental controls were used to ensure that neural modulation was attributable to grip only. These findings, in concert with previous studies demonstrating that V6A neurons are modulated by reach direction and wrist orientation, that lesion of V6A evokes reaching and grasping deficits, and that dorsal premotor cortex contains both reaching and grasping neurons, indicate that the dorsomedial parieto-frontal circuit may play a central role in all phases of reach-to-grasp action. Our data suggest new directions for the modeling of prehension movements and testable predictions for new brain imaging and neuropsychological experiments.