Physiological organization of layer 4 in macaque striate cortex

Abstract

Numerous highly angled electrode penetrations through the opercular region of macaque striate cortex reveal that layers 4A, 4C alpha, and 4C beta--the primary input sublaminae for axons from the lateral geniculate nucleus (LGN)--are retinotopically organized on a fine scale and populated mostly by monocularly driven cells having small receptive fields and lacking orientation selectivity. Layer 4B, which does not receive a direct thalamic input, contains orientationally selective cells, and many of these are also direction selective. To a significant degree the response properties of cells in layers 4C alpha and 4C beta reflect the response properties of their respective afferent inputs, from the magno- and parvocellular laminae of the LGN. Accordingly, cells in layer 4C alpha have lower contrast thresholds and larger minimum response fields than do the cells in layer 4C beta. In contrast to this clear-cut separation, the cells of layer 4A (whose major source of direct LGN input arises from the parvocellular layers) exhibit both high and low contrast thresholds. With regard to the precision of retinotopic mapping that is seen in lamina 4C, it is noteworthy that there is substantial overlap among the minimum response fields of neighboring neurons. Due to a larger mean receptive field size, this overlap is greater in layer 4C alpha than it is in 4C beta. In either sublamina, however, the minimum cortical distance that separates different and nonoverlapping parts of the visual field corresponds closely--within a factor of 2--to the known arborizational spreads of single geniculate afferents.

Innervation patterns of single physiologically identified geniculocortical axons in the striate cortex of the tree shrew.

“…There is no question that the contribution of geniculocortical terminations to ON/OFF and binocular convergence varies considerably across species. For example, in Old World monkeys, neither binocular convergence nor ON/OFF convergence occurs in layer IV (13,20,22), whereas in carnivores both seem to occur (e.g., ref. 15).…”

Functional Analysis of V3A and Related Areas in Human Visual Cortex

“…V3 itself shows motion and direction selectivity in approximately one-half of its neurons (Felleman and Van Essen, 1987;Gegenfurtner et al, 1994). The percentage of motion-selective cells in layer 4B is higher than that in any other known layer of V1 (Dow, 1974;Blasdel and Fitzpatrick, 1984;Hawken et al, 1988), approximately equal to that in V3 (Felleman and Van Essen, 1987;Gegenfurtner et al, 1994). Besides V3, MT is the most prominent extrastriate area that shares a direct input from this layer of V1, and MT is widely accepted to be involved in motion and direction processing.…”

Oriented Axon Projections in Primary Visual Cortex of the Monkey

“…Neurons in layer 3 lie one synapse downstream from the geniculate-receptive layers 4C␤ and 4A, which have few cells with orientation selectivity (Hubel and Wiesel, 1968;Dow, 1974;Bullier and Henry, 1980;Blasdel and Fitzpatrick, 1984;Anderson et al, 1993;Ringach et al, 1997). Layer 4B, the intralaminar projections of which form the stria of Gennari, is also one synapse removed from its geniculate input in layer 4C␣ (Fitzpatrick et al, 1985;Yabuta and Callaway, 1998a).…”

“…Unlike cat V1, where it appears that patterned input from the lateral geniculate nucleus to layer 4 provides the basis for orientation selectivity (Hubel and Wiesel, 1962;Ferster and Miller, 2000), neurons in layer 4C of primate V1 are insensitive to stimulus orientation. Instead, sharp orientation tuning is found in layers 2/3 and 4B, one synapse removed from the thalamic input (Hubel and Wiesel, 1968;Dow, 1974;Bullier and Henry, 1980;Blasdel and Fitzpatrick, 1984;Anderson et al, 1993;Ringach et al, 1997). Consequently, orientation selectivity in primates seems to arise from intracortical circuitry.…”