Structure and function of parallel pathways in the primate early visual system

Abstract

Parallel processing streams in the primate visual system originate from more than a dozen anatomically and functionally distinct types of retinal ganglion cells (RGCs). A central problem in determining how visual information is processed is understanding how each of these RGC types connects to more central structures, including the lateral geniculate nucleus (LGN) of the thalamus and (via the LGN) the primary visual cortex. Nevertheless, the available functional and anatomical evidence linking together specific cell types across these structures is surprisingly indirect. This review evaluates the available evidence and assesses the strength of the many inferences that can be made from these observations. There is strong evidence that parasol RGCs are the provenance of the magnocellular (M) visual pathway and that midget RGCs give rise to the parvocellular (P) pathway. Furthermore, the M and P pathways remain segregated up to the input layer of primary visual cortex. The relationships between the numerous other RGC types and cell types in the LGN remain less certain. and there remains ambiguity about how best to define additional pathways, such as the koniocellular (K) pathway, which probably arise from these other, less common, RGC types.

Figure 1. Connections of retinal ganglion cell types to LGN layers (A) and the functional organization of LGN afferents terminating in primary visual cortex (V1) (B)

A, as described in detail in the main text, midget ganglion cells have red–green colour opponency and connect to parvocellular (P) layers of the LGN. Some midget ganglion cells might have 'blue–OFF' receptive fields. Parasol ganglion cells carry luminance signals to magnocellular (M) layers of the LGN. Small bistratified ganglion cells have 'blue–ON' receptive fields and probably connect to koniocellular (K) neurones located mostly in the intercalated layers of the LGN. In addition there are numerous other ganglion cell types that connect to the LGN, but their functional properties and postsynaptic targets remain unidentified. B, recordings from the afferent axonal arbors of LGN neurones at their sites of termination in V1 have revealed the functional organization of LGN input to V1. Afferents recorded in layer 4Cβ of V1 have red–green colour opponency and arise from LGN P cells. Afferents recorded in layer 4Cα are achromatic and arise from LGN M cells. Afferents recorded in more superficial layers have blue–yellow colour opponency. Blue–OFF afferents are encountered only in layer 4A and might arise from blue–OFF midget ganglion cells via LGN P cells. But it also possible that they might have some other origin. Blue–ON afferents are encountered on layers 3 and 4A and therefore arise (at least in part) from αCAM kinase/calbindin-expressing LGN K cells. A is from Dacey (2000) and B is from Chatterjee & Callaway (2003).