Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams

Abstract

The primate visual system consists of at least two processing streams, one passing ventrally into temporal cortex that is responsible for object vision, and the other running dorsally into parietal cortex that is responsible for spatial vision. How information from these two streams is combined for perception and action is not understood. Visually guided eye movements require information about both feature identity and location, so we investigated the topographic organization of visual cortex connections with frontal eye field (FEF), the final stage of cortical processing for saccadic eye movements. Multiple anatomical tracers were placed either in parietal and temporal cortex or in different parts of FEF in individual macaque monkeys. Convergence from the dorsal and ventral processing streams occurred in lateral FEF but not in medial FEF. Certain extrastriate areas with retinotopic visual field organizations projected topographically onto FEF. The dorsal bank of the superior temporal sulcus projected to medial FEF; the ventral bank, to lateral FEF, and the fundus, throughout FEF. Thus, lateral FEF, which is responsible for generating short saccades, receives visual afferents from the foveal representation in retinotopically organized areas, from areas that represent central vision in inferotemporal cortex and from other areas having no retinotopic order. In contrast, medial FEF, which is responsible for generating longer saccades, is innervated by the peripheral representation of retinotopically organized areas, from areas that emphasize peripheral vision or are multimodal and from other areas that have no retinotopic order or are auditory.

Multisensory anatomical pathways

“…Similarly, the connectivity pattern of the LIP Blatt et al, 1990;Lewis and Van Essen, 2000) is consistent with the multisensory properties reported for LIP neurons (Cohen et al, 2005;Russ et al, 2006;Gottlieb, 2007). The ventral part of LIP connects with areas dealing with spatial information (visual area MT and the auditory caudiomedial area; Andersen et al, 1997), as well as with the frontal eye field (Schall et al, 1995), whereas the dorsal part of LIP is connected with areas responsible for the processing of visual information related to the form of objects in the inferotemporal cortex (ventral ''what" visual pathway). In parallel, the temporal region of the superior temporal sulcus (STS) is connected with the visual occipital cortices (Seltzer and Pandya, 1994) and with the secondary auditory area (area 22 of Brodmann; Pandya and Seltzer, 1982) providing the multimodal properties of neurons in area STP (Bruce et al, 1981;Baylis et al, 1987;Hikosaka et al, 1988).…”

“…In the visual system, density and laminar profile of the connections between visual areas also differ depending on whether they involve the representation of the central or peripheral visual field (Shipp and Zeki, 1989;Kaas and Morel, 1993;Schall et al 1995;Galletti et al 2001;Palmer and Rosa, 2006). Our connectivity data show that heteromodal connections are also specific to the sensory representation.…”

How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades

“…A stimulus may have separate dimensions of color, shape, texture, quantity, and motion, among other factors. The FEF receives inputs from areas that process all of these information types (Schall et a!., 1995a). Separate modules may exist to generate saccades using different stimulus dimensions, because a given input can map to various outputs, depending on which stimulus dimensions are used to guide a saccade (e.g., motion vs. color) as well as the specific decision criteria (e.g., foveate red vs. green objects or leftward vs. rightward moving objects).…”

“…Postsaccadic cells fire phasically immediately after a saccade has been initiated. Schall et al, 1995a.] (B) Visuomovement cells.…”

Shortening and prolongation of saccade latencies following microsaccades

“…This area receives retinotopically-organized input from the visual cortex (Schall et al 1995) and contains cells that show tonic discharge activity during the delay periods in memory-saccade tasks. This activity is spatially specific for the target location and available to the target saccade (Friedman et al 1997;Bruce et al 2004).…”