Michela Gamberini

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‐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.

Cortical Connections of the Visuomotor Parietooccipital Area V6Ad of the Macaque Monkey

Area V6A, a functionally defined region in the anterior bank of the parietooccipital sulcus, has been subdivided into dorsal and ventral cytoarchitectonic fields (V6Ad and V6Av). The aim of this study was to define the cortical connections of the cytoarchitectonic field V6Ad. Retrograde and bidirectional neuronal tracers were injected into the dorsal part of the anterior bank of parietooccipital sulcus of seven macaque monkeys (Macaca fascicularis). The limits of injection sites were compared with those of cytoarchitectonic fields. The major connections of V6Ad were with areas of the superior parietal lobule. The densest labeling was observed in the medial intraparietal area (MIP). Areas PEc, PGm, and V6Av were also strongly connected. Labeled cells were found in medial parietal area 31; in cingulate area 23; in the anterior (AIP), ventral (VIP), and lateral (LIP) intraparietal areas; in the inferior parietal lobule (fields Opt and PG); and in the medial superior temporal area (MST). In the frontal lobe, the main projection originated from F2, although labeled cells were also found in F7 and area 46. Preliminary results obtained from injections in nearby areas PEc and V6Av revealed connections different from those of V6Ad. In agreement with functional data, the strong connections with areas where arm‐reaching activity is represented suggest that V6Ad is part of a parietofrontal circuit involved in the control of prehension, and connections with AIP specifically support an involvement in the control of grasping. Connections with areas LIP and Opt are likely related to the oculomotor activities observed in V6Ad. J. Comp. Neurol. 513:622–642, 2009.

Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study.

The anterior wall of the parieto‐occipital sulcus (POs) of the macaque monkey, classically considered as part of Brodmanns area 19, contains two functionally distinct areas: a ventral, purely visual area, V6, and a dorsal area, V6A, containing visual neurons and neurons related to the control of arm movements. The aim of this study was to establish whether areas V6 and V6A, so far identified only on a functional basis, have a cytoarchitectonic counterpart. The cytoarchitectonic analysis of 13 hemispheres from ten macaque brains, cut along different planes of section, showed that the anterior wall of the POs contains three distinct areas. One is located in the ventralmost part of the wall, another in the dorsalmost part of the wall, and the third occupies an intermediate position. The ventralmost region displays architectonic features typical of the occipital cytoarchitectonic domain, whereas the two dorsal areas display architectonic features typical of the posterior parietal cortex. Analysis of myeloarchitecture and of the distribution of SMI‐32 immunoreactivity confirmed the cytoarchitectonic parcellation. Correlation of cytoarchitectonic maps with functional and hodological data strongly suggests that the ventral region corresponds to area V6, whereas the other two regions correspond to different subsectors of V6A, here named V6Av and V6Ad, respectively. The present data are in line with electrophysiological and hodological data, which suggest that area V6 is a classic extrastriate area, whereas V6A is an area of the posterior parietal cortex. They also suggest that V6A includes two separate cortical subdivisions, a view supported by preliminary functional and hodological data that needs further confirmation.

Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas

We describe the organization of the dorsolateral frontal areas in marmoset monkeys using a combination of architectural methods (Nissl, cytochrome oxidase, and myelin stains) and injections of fluorescent tracers in extrastriate areas (the second visual area [V2], the dorsomedial and dorsoanterior areas [DM, DA], the middle temporal area and middle temporal crescent [MT, MTc], and the posterior parietal cortex [area 7]). Cytoarchitectural field 8 comprises three subdivisions: 8Av, 8Ad, and 8B. The ventrolateral subdivision, 8Av, forms the principal source of frontal projections to the “dorsal stream,” having connections with each of the injected visual areas. The cytoarchitectural characteristics of 8Av suggest that this subdivision corresponds to the marmosets frontal eye field. The intermediate subdivision of area 8 (8Ad) has efferent projections to area 7, while the dorsomedial subdivision (8B) has few or no connections with extrastriate cortex. Area 46, located rostrolateral to area 8Av, has substantial connections with the medial extrastriate areas (DM, DA, and area 7) and with MT, while the cortex lateral to 8Av (area 12/45) projects primarily to MT and to the MTc. The rostromedial prefrontal (area 9) and frontopolar (area 10) regions have very few extrastriate projections. Finally, cells in dorsal area 6 (6d) have sparse projections to DM, MT, and the MTc, as well as strong projections to DA and to area 7. These results illuminate aspects of the evolutionary development of the primate frontal cortex, and serve as a basis for further research into cognitive functions using a marmoset model. J. Comp. Neurol. 495:149–172, 2006.

Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex

The dorsomedial area (DM), a subdivision of extrastriate cortex characterized by heavy myelination and relative emphasis on peripheral vision, remains the least understood of the main targets of striate cortex (V1) projections in primates. Here we placed retrograde tracer injections encompassing the full extent of this area in marmoset monkeys, and performed quantitative analyses of the numerical strengths and laminar patterns of its afferent connections. We found that feedforward projections from V1 and from the second visual area (V2) account for over half of the inputs to DM, and that the vast majority of the remaining connections come from other topographically organized visual cortices. Extrastriate projections to DM originate in approximately equal proportions from adjacent medial occipitoparietal areas, from the superior temporal motion-sensitive complex centered on the middle temporal area (MT), and from ventral stream-associated areas. Feedback from the posterior parietal cortex and other association areas accounts for <10% of the connections. These results do not support the hypothesis that DM is specifically associated with a medial subcircuit of the dorsal stream, important for visuomotor integration. Instead, they suggest an early-stage visual-processing node capable of contributing across cortical streams, much as V1 and V2 do. Thus, although DM may be important for providing visual inputs for guided body movements (which often depend on information contained in peripheral vision), this area is also likely to participate in other functions that require integration across wide expanses of visual space, such as perception of self-motion and contour completion.

Somatosensory Cells in Area PEc of Macaque Posterior Parietal Cortex

PEc is an area defined on cytoarchitectural grounds, located in the posterior part of the superior parietal lobule of macaque brain (Pandya and Seltzer, 1982). The aim of this work was to assess whether passive somatosensory stimulation elicited responses in PEc neurons. Extracellular recordings were performed in three awake Macaca fascicularis. Passive somatosensory stimulation was performed in darkness, and eye movements were monitored continuously. Recording sites were assigned to different areas according to the cytoarchitectonic criteria described by Pandya and Seltzer (1982) and Luppino et al. (2005). Only recording sites within the limits of the cytoarchitecturally defined area PEc were taken into account in this work. Of 147 PEc cells, 83 (56%) were modulated by passive somatosensory stimulation. The majority of them (73%) responded to joint rotations, and 24% responded to tactile skin stimulation. The majority of PEc somatosensory responses (90%) were evoked by contralateral stimulation. Joint-modulated cells were mostly activated by the upper limbs (82%). The majority of tactile receptive fields (61%) were located on the arms, and a minority was located on the legs and trunk. One-half of PEc somatosensory cells were polysensory, because they were sensitive to visual stimulation. The majority of PEc somatosensory cells were activated by active reaching movements. Somatosensory cells, somatosensory submodalities, and body part representations were not clustered in PEc subregions; in other words, PEc does not show a somatotopic organization. Although the caudal sector of the superior parietal lobule has been traditionally considered as a somatosensory area, this is the first demonstration of the presence of somatosensory cells in this cortical region.

Resolving the organization of the New World monkey third visual complex: the dorsal extrastriate cortex of the marmoset (Callithrix jacchus).

We tested current hypotheses on the functional organization of the third visual complex, a particularly controversial region of the primate extrastriate cortex. In anatomical experiments, injections of retrograde tracers were placed in the dorsal cortex immediately rostral to the second visual area (V2) of New World monkeys (Callithrix jacchus), revealing the topography of interconnections between the “third tier” cortex and the primary visual area (V1). The data indicate the presence of a dorsomedial area (DM), which represents the entire upper and lower quadrants of the visual field, and which receives strong, topographically organized projections from the superficial layers of V1. The visuotopic organization and boundaries of DM were confirmed by electrophysiological recordings in the same animals and by architectural characteristics which were distinct from those found in ventral extrastriate cortex rostral to V2. There was no electrophysiological or histological evidence for a transitional area between V2 and DM. In particular, the central representation of the upper quadrant in DM was directly adjacent to the representation of the horizontal meridian that marks the rostral border of V2. The present results argue in favor of the hypothesis that the third visual complex in New World monkeys contains different areas in its dorsal and ventral components: area DM, near the dorsal midline, and a homolog of area 19 of other mammals, located more lateral and ventrally. The characteristics of DM suggest that it may correspond to visual area 6 (V6) of Old World monkeys. J. Comp. Neurol. 483:164–191, 2005.