Topography of the afferent connectivity of area 17 in the macaque monkey: A double‐labelling study
Authors: Perkel David J. , Bullier Jean , Kennedy Henry 
Published: January 2005

The various structures afferent to area 17 (or V1) of the macaque monkey have widely differing retinotopic organizations. It is likely that these difference are reflected in the topographic organization of the projection from these structures to area V1. We have investigated this issue by placing side‐by‐side injections of two retrograde fluorescent tracers, fast blue and diamidino yellow, in V1. By examining the extent of mixing of the two populations of singly labelled cells and the presence of doubly labelled cells, in different structures, we have characterized the topography of each projection in terms of the size of its axonal arborization and the amount of convergence and divergence.

The afferents from the lateral geniculate nucleus (LGN) and from the pulvinar are organized in a point‐to‐point fashion. The maximum extent of axonal arborization of these afferents is 0.5 mm and these projections demonstrate little scatter (i.e., neighboring LGN neurons project to adjacent regions of V1). The other two subcortical structures examined, the claustrum and the intralaminar nuclei, demonstrate a much larger scatter and wider axonal arborizations in their projections to V1 than do the LGN and pulvinar.

Two‐dimensional reconstructions were made of the distribution of labelled neurons in extrastriate cortical areas. Using the separation between patches of labelled cells and transitions in myelin‐stained sections, we have identified seven separate cortical regions containing labelled cells. Two of these can be identified as area V2 and the middle temporal visual area (MT). Three other regions correspond to areas V3, V3A and V4t. Finally, two more regions of labelling have been distinguished that belong to area V4. These results demonstrate that, at least within the central 6° of visual field, all the presently known extrastriate visual cortical areas project to V1. This result is interesting in view of the fact that only a few extrastriate cortical areas are reported to receive afferents from V1.

Three groups of cortical areas can be distinguished on the basis of the characteristics of their cortical connections to V1. The first group contains area V2, V3, and the posterior region of V4. These areas project to V1 with infra‐ as well as supragranular layer neurons and show limited axonal arborization and scatter in the projection. The second group consists of two regions of labelling in the superior temporal sulcus corresponding to V4t and MT and another on the annectant gyrus (V3A). These regions contain almost exclusively infragranular labelling and show wide axonal‐arborization and scatter in their projections to V1. Finally, the neurons on the prelunate gyrus (V4) appear to have characteristics intermediate between the first two groups.

Examination of the literature reveals that there is a relationship between the receptive field (RF) properties of neurons in different structures afferent to V1 and the geometry of their projection. Structures such as the LGN with small RF size and scatter display point‐to‐point projections to V1. Structures such as the claustrum or area MT that have larger RF size and greater scatter exhibit larger degrees of divergence in their projections to V1.