Dieter F. Kutz

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.

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.

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

‘Arm‐reaching’ neurons in the parietal area V6A of the macaque monkey

In previous experiments we have found that several cells of area V6A in the macaque superior parietal lobule were activated by small and stereotyped movements of the arms (C. Galletti, P. Fattori, D. F. Kutz & P. P. Battaglini, Eur. J. Neurosci., 1997, 9, 410). This behaviour was not accounted for by retinal information, nor by somatosensory inputs from the arms. We now want to investigate whether V6A neurons are modulated by purposeful movements aimed at reaching visual targets or targets located outside the field of view. V6A neuronal activity was collected while monkeys performed arm movements during an instructed‐delay reaching task in darkness. The task required the animal to reach out for a visual target in the peripersonal space and to bring the hand back to its body. Quantitative analysis of neuronal activity carried out on 55 V6A neurons showed that: (i) the great majority of neurons (71%) was significantly modulated during the execution of arm movements; (ii) 30% of neurons were significantly modulated during preparation of reaching; and (iii) modulations during both execution and preparation of reaching occurred in the absence of any visual feedback and were not due to eye movements. V6A reach‐related neurons could be useful in guiding the hand to reach its target with or without visual feedback.

Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey.

We recorded neural activity from the medial parieto‐occipital area V6A while three monkeys performed an instructed‐delay reaching task in the dark. Targets to be reached were in different spatial positions. Neural discharges were recorded during reaching movements directed outward from the body (towards visual objects), during the holding phase (when the hand was on the target) and during inward movements of the hand towards the home button (which was near the body and outside the field of view). Reach‐related activity was observed in the majority of 207 V6A cells, during outward (78%) and inward (65%) movements as well as during the holding phase (62%). Most V6A reaching neurons (84%) were modulated in more than one phase of the task. The reach‐related activity in V6A could depend on somatosensory inputs and/or on corollary discharges from the dorsal premotor cortex. Although visual and oculomotor inputs are known to have a strong influence on V6A activity, we excluded the possibility that the reach‐related activity which we observed was due to visual stimulation and/or oculomotor activity. Reach‐related activity for movements towards different locations was spatially modulated during outward (40%) and inward (47%) reaching movements. The position of the hand/arm in space modulated about 40% of V6A cells. Preferred reach directions and spatial locations were represented uniformly across the workspace. These data suggest that V6A reach‐related neurons are able to code the direction of movement of the arm and the position of the hand/arm in space. We suggest that the V6A reach‐related neurons are involved in the guidance of goal‐directed arm movements, whether these actions are visually guided or not.

Influence of arm movements on saccades in humans

When reaching for an object we usually look at it before we touch it with the hand. This often unconscious eye movement prior to the arm movement allows guiding of the final part of the hand trajectory by visual feedback. We examined the temporal and spatial coordination of this control system by psychophysical measurements of eye and arm movements of naive human subjects looking or looking and pointing as fast as possible to visual targets in physical and virtual‐reality setups. The reaction times of saccades to a step‐displaced target were reduced, and the number of corrective saccades decreased, when the subject had to produce a corresponding simultaneous hand movement to the same target. The saccadic reaction time was increased when saccade and hand movement went in opposite directions. In a double‐step task the reaction time for the second saccade was longer than for the first. Co‐use of the hand leads to an additional increase of saccadic reaction time. Taken together this study shows an improvement in initial saccades if they are accompanied by hand movements to the same target. This effect might ensure that the reach target is foveated early and accurately enough to support the visual feedback control of the hand near the target. Longer reaction times for the second saccade to double‐step displaced targets might reflect a saccadic refractory time intensified by simultaneous arm movements. These results are discussed in the light of recent findings from our laboratory on saccade‐ and reach‐related neurons in the superior colliculus of macaque monkeys.

Somatosensory cells in the parieto-occipital area V6A of the macaque

The aim of this study was to assess whether neurones of area V6A, a part of Brodmanns area 19, are modulated by passive somatosensory stimulations. Extracellular activity was recorded in four awake Macaca fascicularis while passive tactile stimulations of the skin and passive rotations of the joints were performed in complete darkness and under eye movement control. Out of 240 V6A units, 78 (32%) were modulated by somatosensory stimulations. The majority of somatic receptive fields were located on both proximal and distal parts of the contralateral arm. V6A somatosensory cells may play a role in the feedback control of the actual state of the arm while reaching its target in peripersonal space.

The relationship between V6 and PO in macaque extrastriate cortex.

The cerebral cortex of three macaque monkeys, electrophysiologically studied in chronic preparations in order to recognize functionally the medial parieto‐occipital area V6, was reconstructed using the software CARET. Locations of cells recorded from area V6 (n = 553) and from neighbouring cortical areas V2/V3 and V6A (n = 1341) were displayed on surface‐based reconstructions of individual brains, and on a surface‐based atlas of the macaque cerebral cortex. Results show that area V6 occupies the ventral part and fundus of the parieto‐occipital sulcus, as well as the ventral part of the precuneate cortex. V6 borders areas V2/V3 posteriorly and laterally, and area V6A anteriorly. The visualization of individual cases on a common template (atlas), and the use of atlas datasets, allowed us to compare data coming from different individuals and different laboratories. In particular, a comparison of the location and extent of the medial parieto‐occipital areas V6 and PO indicates that area PO occupies different locations according to different authors but in general includes parts of both areas V6 and V6A. We therefore suggest that the term V6 is a more appropriate designation of the visuotopically‐organized area located on the anterior wall of the parieto‐occipital sulcus.