Sophia Bakola

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.

Cortical Connections of Parietal Field PEc in the Macaque: Linking Vision and Somatic Sensation for the Control of Limb Action

The cortical projections to the caudal part of the superior parietal lobule (area PEc) were studied in 6 cynomolgus monkeys using fluorescence tracers. Significant numbers of labeled cells were found in a restricted network of parietal, mesial, and frontal areas. Quantitative analysis demonstrated that approximately 30% of the total projection neurons originated in the adjacent areas of the dorsocaudal part of the superior parietal lobule (areas PE and V6A). The medial bank of the intraparietal sulcus, inferior parietal lobule, and frontal lobe (mainly the dorsocaudal part of premotor area F2) each contributed approximately 15% of the projection neurons. About 15% of the labeled neurons were located in the posterior cingulate area (PEci) and another 10% in other areas of the mesial surface of the hemisphere. Based on these data, we suggest that PEc processes information about the position of the limbs. The specific anatomical links between PEc and motor and premotor areas that host a representation of the lower limbs, together with the link with vestibular cortex and with areas involved in the analysis of optic flow and spatial navigation, imply a role for PEc in locomotion and coordinated limb movement in the environment.

Cortical Connections of Area V6Av in the Macaque: A Visual-Input Node to the Eye/Hand Coordination System

The goal of the present study was to elucidate the corticocortical afferent connections of area V6Av, the ventral subregion of area V6A, using retrograde neuronal tracers combined with physiological and cytoarchitectonic analyses in the macaque monkey. The results revealed that V6Av receives many of its afferents from extrastriate area V6, and from regions of areas V2, V3, and V4 subserving peripheral vision. Additional extrastriate visual projections originate in dorsal stream areas MT and MST. Area V6Av does not receive projections directly from V1; such connections were only observed when the injection sites crossed into area V6. The strongest parietal lobe afferents originate in fields V6Ad, PGm, MIP (medial intraparaietal), and PG, with frontal lobe afferents originating from the frontal eye field, caudal area 46, and the rostral subdivision of the dorsal premotor area (F7). A comparison of their respective connections supports the view that V6Av is functionally distinct from adjacent areas (V6 and V6Ad). The strong afferents from V6 and other extrastriate areas are consistent with physiological data that suggest that V6Av is primarily a visual area, supporting the notion that V6Av is part of a dorsomedial cortical network performing fast form and motion analyses needed for the visual guidance of action.

Cortical Connectivity Suggests a Role in Limb Coordination for Macaque Area PE of the Superior Parietal Cortex

In macaques, superior parietal lobule area 5 has been described as occupying an extensive region, which includes the caudal half of the postcentral convexity as well as the medial bank of the intraparietal sulcus. Modern neuroanatomical methods have allowed the identification of various areas within this region. In the present study, we investigated the corticocortical afferent projections of one of these subdivisions, area PE. Our results demonstrate that PE, defined as a single architectonic area that contains a topographic map of the body, forms specific connections with somatic and motor fields. Thus, PE receives major afferents from parietal areas, mainly area 2, PEc, several areas in the medial bank of the intraparietal sulcus, opercular areas PGop/PFop, and the retroinsular area, frontal afferents from the primary motor cortex, the supplementary motor area, and the caudal subdivision of dorsal premotor cortex, as well as afferents from cingulate areas PEci, 23, and 24. The presence and relative strength of these connections depend on the location of injection sites, so that lateral PE receives preferential input from anterior sectors of the medial bank of intraparietal sulcus and from the ventral premotor cortex, whereas medial PE forms denser connections with area PEc and motor fields. In contrast with other posterior parietal areas, there are no projections to PE from occipital or prefrontal cortices. Overall, the sensory and motor afferents to PE are consistent with functions in goal-directed movement but also hint at a wider variety of motor coordination roles.

Patterns of cortical input to the primary motor area in the marmoset monkey

In primates the primary motor cortex (M1) forms a topographic map of the body, whereby neurons in the medial part of this area control movements involving trunk and hindlimb muscles, those in the intermediate part control movements involving forelimb muscles, and those in the lateral part control movements of facial and other head muscles. This topography is accompanied by changes in cytoarchitectural characteristics, raising the question of whether the anatomical connections also vary between different parts of M1. To address this issue, we compared the patterns of cortical afferents revealed by retrograde tracer injections in different locations within M1 of marmoset monkeys. We found that the entire extent of this area is unified by projections from the dorsocaudal and medial subdivisions of premotor cortex (areas 6DC and 6M), from somatosensory areas 3a, 3b, 1/2, and S2, and from posterior parietal area PE. While cingulate areas projected to all subdivisions, they preferentially targeted the medial part of M1. Conversely, the ventral premotor areas were preferentially connected with the lateral part of M1. Smaller but consistent inputs originated in frontal area 6DR, ventral posterior parietal cortex, the retroinsular cortex, and area TPt. Connections with intraparietal, prefrontal, and temporal areas were very sparse, and variable. Our results demonstrate that M1 is unified by a consistent pattern of major connections, but also shows regional variations in terms of minor inputs. These differences likely reflect requirements for control of voluntary movement involving different body parts. J. Comp. Neurol. 522:811–843, 2014.

Cortical and thalamic projections to cytoarchitectural areas 6Va and 8C of the marmoset monkey: Connectionally distinct subdivisions of the lateral premotor cortex

We studied the afferent connections of two cytoarchitectural subdivisions of the caudolateral frontal cortex, areas 6Va and 8C, in marmoset monkeys. These areas received connections from the same set of thalamic nuclei, including main inputs from the ventral lateral and ventral anterior complexes, but differed in their patterns of corticocortical connections. Areas 8C and 6Va had reciprocal interconnections, and received similar proportions of afferents from premotor areas 6M and 6DC, and from the prefrontal cortex. However, area 8C received stronger inputs from frontal areas that have been implicated in oculomotor functions, whereas area 6Va received stronger projections from the primary motor area. Somatosensory projections to area 6Va were generally stronger than those to area 8C, and originated from several areas; in contrast, only the second somatosensory area (S2) sent major inputs to area 8C. Finally, although both 6Va and 8C received major inputs from the rostral posterior parietal cortex (putative homologs of areas PE, PF, and PFG), area 8C also received a variety of smaller connections from posterior midline, caudal posterior parietal, and extrastriate areas. Statistical analyses revealed that the pattern of connections of area 8C is more akin to that characterizing a premotor area, rather than a prefrontal area. We conclude that cytoarchitectural area 6Va in the marmoset is similar to ventral premotor areas identified in other simian primates, and that area 8C corresponds to a specialized subdivision of the caudal premotor complex where visual information for the guidance of movements is likely to be emphasized. J. Comp. Neurol. 523:1222–1247, 2015.

The place code of saccade metrics in the lateral bank of the intraparietal sulcus.

The lateral intraparietal area (LIP) of monkeys is known to participate in the guidance of rapid eye movements (saccades), but the means it uses to specify movement variables are poorly understood. To determine whether area LIP devotes neural space to encode saccade metrics spatially, we used the quantitative [14C]deoxyglucose method to obtain images of the distribution of metabolic activity in the intraparietal sulcus (IPs) of rhesus monkeys trained to repeatedly execute saccades of the same amplitude and direction for the duration of the experiment. Different monkeys were trained to perform saccades of different sizes and in different directions. A clear topography of saccade metrics was found in the cytoarchitectonically identified area LIP ventral (LIPv) contralateral to the direction of the eye movements. We demonstrate that the representation of the vertical meridian runs parallel to the fundus of the IPs and that it is not orthogonal to the representation of the horizontal meridian. Instead, the latter runs through the middle of LIPv parallel to its border with area LIP dorsal (LIPd). The upper part of oculomotor space is represented rostrally and dorsally relative to the horizontal meridian toward the LIPv–LIPd border, whereas the lower part of oculomotor space is represented caudally and ventrally toward the caudal edge of the IPs. Saccade amplitude is also represented in an orderly manner.

Saccade-Related Information in the Superior Temporal Motion Complex: Quantitative Functional Mapping in the Monkey

Although the role of the motion complex [cortical areas middle temporal (V5/MT), medial superior temporal (MST), and fundus of the superior temporal (FST)] in visual motion and smooth-pursuit eye movements is well understood, little is known about its involvement in rapid eye movements (saccades). To address this issue, we used the quantitative 14C-deoxyglucose method to obtain functional maps of the cerebral cortex lying in the superior temporal sulcus of rhesus monkeys executing saccades to visual targets and saccades to memorized targets in complete darkness. Fixational effects were observed in MT-foveal, FST, the anterior part of V4-transitional (V4t), and temporal-occipital areas. Saccades to memorized targets activated areas V5/MT, MST, and V4t, which were also activated for saccades to visual targets. Regions activated in the light and in the dark overlapped extensively. In addition, saccades to visual targets activated areas FST and the intermediate part of the polysensory temporal-parietal-occipital area. Cortical activity related to visually guided saccades could be explained, at least in part, by visual motion. Because only oculomotor signals can account for the equally robust activations induced by memory saccades in complete darkness, we suggest that areas V5/MT, MST, and V4t receive and/or process saccade-related oculomotor information.

Thalamic projections to visual and visuomotor areas (V6 and V6A) in the Rostral Bank of the parieto-occipital sulcus of the Macaque

The medial posterior parietal cortex of the primate brain includes different functional areas, which have been defined based on the functional properties, cyto- and myeloarchitectural criteria, and cortico-cortical connections. Here, we describe the thalamic projections to two of these areas (V6 and V6A), based on 14 retrograde neuronal tracer injections in 11 hemispheres of 9 Macaca fascicularis. The injections were placed either by direct visualisation or using electrophysiological guidance, and the location of injection sites was determined post mortem based on cyto- and myeloarchitectural criteria. We found that the majority of the thalamic afferents to the visual area V6 originate in subdivisions of the lateral and inferior pulvinar nuclei, with weaker inputs originating from the central densocellular, paracentral, lateral posterior, lateral geniculate, ventral anterior and mediodorsal nuclei. In contrast, injections in both the dorsal and ventral parts of the visuomotor area V6A revealed strong inputs from the lateral posterior and medial pulvinar nuclei, as well as smaller inputs from the ventrolateral complex and from the central densocellular, paracentral, and mediodorsal nuclei. These projection patterns are in line with the functional properties of injected areas: “dorsal stream” extrastriate area V6 receives information from visuotopically organised subdivisions of the thalamus; whereas visuomotor area V6A, which is involved in the sensory guidance of arm movement, receives its primary afferents from thalamic nuclei that provide high-order somatic and visual input.

Uniformity and Diversity of Cortical Projections to Precuneate Areas in the Macaque Monkey: What Defines Area PGm?

We report on the corticocortical connections of areas on the mesial surface of the macaque posterior parietal cortex, based on 10 retrograde tracer injections targeting different parts of the precuneate gyrus. Analysis of afferent connections supported the existence of two areas: PGm (also known as 7 m) and area 31. Both areas received major afferents from the V6A complex and from the external subdivision of area 23, but they differed in most other aspects. Area 31 showed greater emphasis on connections with premotor and parietal sensorimotor areas, whereas PGm received a greater proportion of its afferents from visuomotor structures involved in spatial cognition (including the lateral intraparietal cortex, inferior parietal lobule, and the putative visual areas in the ventral part of the precuneus). Medially, the anterior cingulate cortex (area 24) preferentially targeted area 31, whereas retrosplenial areas preferentially targeted PGm. These results indicate that earlier views on the connections of PGm were based on tracer injections that included parts of adjacent areas (including area 31), and prompt a reassessment of the limits of PGm. Our findings are compatible with a primary role of PGm in visuospatial cognition (including navigation), while supporting a role for area 31 in sensorimotor planning and coordination.