Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque

Abstract

The visual receptive field physiology and anatomical connections of the lateral intraparietal area (area LIP), a visuomotor area in the lateral bank of the inferior parietal lobule, were investigated in the cynomolgus monkey (Macaca fascicularis). Afferent input and physiological properties of area 5 neurons in the medial bank of the intraparietal sulcus (i.e., area PEa) were also determined. Area LIP is composed of two myeloarchitectonic zones: a ventral zone (LIPv), which is densely myelinated, and a lightly myelinated dorsal zone (LIPd) adjacent to visual area 7a. Previous single-unit recording studies in our laboratory have characterized visuomotor properties of area LIP neurons, including many neurons with powerful saccade-related activity. In the first part of the present study, single-unit recordings were used to map visual receptive fields from neurons in the two myeloarchitectonic zones of LIP. Receptive field size and eccentricity were compared to those in adjacent area 7a. The second part of the study investigated the cortico-cortical connections of area LIP neurons using tritiated amino acid injections and fluorescent retrograde tracers placed directly into different rostrocaudal and dorsoventral parts of area LIP. The approach to area LIP was through somatosensory area 5, which eliminated the possibility of diffusion of tracers into area 7a. Unlike many area 7a receptive fields, which are large and bilateral, area LIP receptive fields were much smaller and exclusively confined to the contralateral visual field. In area LIP, an orderly progression in visual receptive fields was evident as the recording electrode moved tangentially to the cortical surface and through the depths of area LIP. The overall visual receptive field organization, however, yielded only a rough topography with some duplications in receptive field representation within a given rostrocaudal or dorsoventral part of LIP. The central visual field representation was generally located more dorsally and the peripheral visual field more ventrally within the sulcus. The lower visual field was represented more anteriorly and the upper visual field more posteriorly. In LIP, receptive field size increased with eccentricity but with much variability within the sample. Area LIPv was found to have reciprocal cortico-cortical connections with many extrastriate visual areas, including the parieto-occipital visual area PO; areas V3, V3A, and V4; the middle temporal area (MT); the middle superior temporal area (MST); dorsal prelunate area (DP); and area TEO (the occipital division of the intratemporal cortex). Area LIPv is also connected to area TF in the lateral posterior parahippocampal gyrus. Although area LIPd has many of the same cortico-cortical connections as LIPv, some differences were apparent. Area LIPd and not LIPv has connections with visual areas TEa and TEm (anterior and medial divisions of the intratemporal cortex) and with multimodal area IPa (subdivision of association cortex in caudal bank of superior temporal cortex) in the superior temporal sulcus. A topographic relationship between rostrocaudal parts of area LIP (including both LIPv and LIPd) and the lateromedial parts of prefrontal cortex across areas 8a (frontal eye fields) and the medial portion of area 46 was also apparent. Intrinsic connections of LIP with other areas in the inferior parietal lobule included a feedforward projection to area 7a and connections with the bimodal ventral intraparietal area (VIP) as well as with somatosensory area 7b (PF). Some retrogradely labeled cells were seen in area 5, but this projection was not confirmed by control injections placed in the medial bank of the intraparietal sulcus (area PEa). An interesting observation was that the input into areas PEa and LIP from parieto-occipital visual areas (medial dorsal parietal area (blDPl and area PO) was found to be topographically organized such that MDP and the dorsal part of PO project to area PEa, while ventral PO and a few MDP neurons project to the opposite bank in LIP. This “visual” input to area PEa was also seen in single-unit recordings in area 5 in wlhich a small number of visually responsive cells were identified Le., 7 of 204 neurons). All remaining neurons mapped in area 5 were highly responsive to joint position, movement, and/or touch. These anatomical and physiological data demonstrate that area LIP is a unique visual area in posterior parietal cortex, with histological, anatomical, and physiological properties different from other areas in the inferior parietal lobule. Analysis of feedforward and feedback projections suggests that area LIP occupies a high position in the overall hierarchy of extrastriate visual processing areas in the macaque brain.