Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns

Abstract

Cortical connections were investigated by restricting injections of WGA-HRP to different parts of the middle temporal visual area, MT, in squirrel monkeys, owl monkeys, marmosets, and galagos. Cortex was flattened and sectioned tangentially to facilitate an analysis of the areal patterns of connections. In the experimental cases, brain sections reacted for cytochrome oxidase (CO) or stained for myelin were used to delimit visual areas of occipital and temporal cortex and visuomotor areas of the frontal lobe. Major findings are as follows: (1) The architectonic analysis suggests that in addition to the commonly recognized visual fields, area 17 (V-I), area 18 (V-II), and MT, all three New World monkeys and prosimian galagos have visual areas DL, DI, DM, MST, and FST. (2) Measurements of the size of these areas indicate that about a third of the neocortex in these primates is occupied by the eight visual areas, but they occupy a somewhat larger proportion of neocortex in the diurnal marmosets and squirrel monkeys than the nocturnal owl monkeys and galagos. The diurnal primates also have proportionally more neocortex devoted to areas 17, 18, and DL and less to MT. These differences are compatible with the view that diurnal primates are more specialized for detailed object and color vision. (3) In all four primates, restricted locations in MT receive major inputs from short meandering rows of neurons in area 17 and several bands of neurons in area 18. (4) Major feedforward projections of MT are to two visual areas adjoining the rostral half of MT, areas MST and FST. Other ipsilateral connections are with DL, DI, and in some cases DM, parts of inferotemporal (IT) cortex, and posterior parietal cortex. (5) In squirrel monkeys, where injection sites varied from caudal to rostral MT, caudal parts of MT representing central vision connect more densely to DL and IT than other parts. Both DL and IT cortex emphasize central vision. (6) In the frontal lobe, MT has dense connections with the frontal ventral area (FV), but not with the frontal eye field (FEF). (7) Callosal connections of MT are most dense with matched locations in MT of the other hemisphere, rather than with the outer boundary of MT representing the vertical meridian. Targets of sparser callosal connections include FST, MST, and DL. The results support the conclusions that (1) prosimian primates and New World monkeys have at least ten visual and visuomotor areas in common, (2) the connections of MT are remarkably consistent across four species of primates, (3) the anatomical segregation of visual subsystems in areas 17 and 18 is common to all primates, (4) connections from the part of MT representing central vision with visual areas emphasizing central vision are more dense, and (5) MT and the associated fields MST and FST occupy proportionally more cortex in nocturnal than diurnal primates.