Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule

Abstract

The anatomical and functional organization of the inferior parietal lobule was investigated in macaque monkeys by using anterograde and retrograde anatomical tracing techniques and single cell recording techniques in awake, behaving monkeys. The connections of areas 7a and 7b, and of two previously unexplored areas, the lateral intraparietal area (LIP) and the dorsal prelunate area (DP), were examined in detail. Functional mapping experiments were performed in all four areas. Prior to this study the pathways for visual input to area 7a were unclear. In these experiments we found several direct projections from extrastriate visual areas, including the lateral intraparietal (LIP), dorsal prelunate (DP), parieto‐occipital (PO), and medial superior temporal (MST) areas into area 7a. Using the observed laminar patterns of connections between areas 7a, LIP, and DP and other extrastriate cortical areas, we were able to construct a hypothetical flow of visual information processing from striate cortex to area 7a. A broader hierarchy was also produced, which relates the positions of areas 7a, 7b, LIP, and DP to various cortical fields in the parietal, temporal, and frontal lobes. By combining single cell recording techniques in trained monkeys with anatomical tracing techniques, we have parcelled the inferior parietal lobule into several subdivisions on the basis of both anatomical and physiological grounds. A clear segregation of visual and somatosensory responses was found in the inferior parietal lobule with areas 7a, LIP, and DP being visual and visual‐motor and area 7b being primarily somatosensory. A similar segregation was found anatomically with areas 7a LIP, and DP being interconnected primarily with other visual cortical areas and area 7b being connected with several somatosensory areas. Area 7b was also found to connect to a few visual cortical areas, and these connections likely account for the small but consistent number of visually responsive cells that are found in this region. Areas LIP, DP, and 7a differed in receptive field and saccade‐related properties. Area 7a visual receptive fields were very large and usually bilateral with a small but significant number of them having receptive field centers in the ipsilateral visual field. Area DP and LIP receptive fields were smaller and the receptive field peaks were almost always confined to the contralateral visual field. Areas 7a, DP, and LIP all contained cells with saccade‐related responses; however, in area 7a there were fewer saccade cells than area LIP, and presaccadic responses were only observed in area LIP. Consistent with its functional specialization for saccades, area LIP was found to be strongly interconnected with areas involved in saccadic eye movements, including the frontal eye fields and intermediate layers of the superior colliculus, whereas area 7a had only weak connections to the frontal eye fields and had no detectable projection to the superior colliculus. Areas LIP, 7a, and DP neurons were found to have eye‐position‐related activity. Extensive quantitative experiments showed the distributions of the slopes and directions of the gaze fields were similar in areas 7a and LIP, but the intercepts were larger for area LIP. Area 7a was found to be connected to at least 22 cortical areas, including MST, superior temporal polysensory (STP), fundus superior temporal (FST), inferotemporal (IT), lateral and medial T F (TF1, TFm) areas, and TEO in the temporal lobe; LIP, DP, PO, medial intraparietal (MIP), posterior intraparietal (PIP), medial dorsal parietal (MDP), medial PG (PGm), and 7b areas in the parieto‐occipital cortex; areas Ba, 46,45,11, and supplementary eye fields (SEF) in the frontal lobe; and areas LC and LA in the cingulate gyrus. Area 7b was found to be connected to area 5; the granular insula (IG), PGm, LC, LA, MDP, MST, PO, STP, and IT areas, and areas 45, 6, and 12. Area LIP had corticocortical connections with the PO, DP, 7a, MST, middle temporal (MT), V4, dorsal and ventral V3 (V3d, V ∼ V ), V3A, TEO, TF, 8a, and 46 areas. Area DP was connected to V3A, LIP, 7a, V4, MST, PO, 46, and 8a. All corticocortical connections were reciprocal. The view that emerges from this study is of a densely interconnected network of connections between large numbers of brain regions with each cortical area, including areas 7a, 7b, LIP, and DP, being a single node in this highly distributed and interactive network. An important goal is to determine what different computations are being performed at each node in this network.