Optical imaging of visually evoked responses in the middle temporal area after deactivation of primary visual cortex in adult primates

Abstract

The middle temporal area (MT) is a visual area in primates with direct and indirect inputs from the primary visual cortex (V1), a role in visual motion perception, and a suggested role in ''blindsight.'' When V1 is deactivated, some studies report continued activation of MT neurons, which has been attributed to an indirect pathway to MT from the superior colliculus. Here we used muscimol to deactivate V1 while optically imaging visually evoked activity in MT in two primates, owl monkeys and galagos, where MT is exposed on the brain surface. The partial loss of V1 inputs abolished all or nearly all evoked activity in the retinotopically matched part of MT. Low levels of activation that persisted in portions of MT that were unstimulated or retinotopically congruent with the blocked portion of V1 appeared to reflect the spread of activity from stimulated to unstimulated parts of MT. Thus, a significant pathway based on the superior colliculus was not demonstrated.V1 lesion ͉ blindsight ͉ muscimol ͉ intrinsic connections T he middle temporal area (MT, also known as V5) is a visual area in the upper temporal lobe of primates that contains a very high proportion of neurons selective for the direction of motion (1, 2) and the orientation of moving gratings (3, 4) and clearly inf luences motion perception (5). Although major inputs to MT are from the primary visual cortex (V1) and areas dependent on V1 for visual activation, such as V2 (6, 7), the effects of lesions or cooling of V1 on the responsiveness of neurons in MT have been inconsistent and difficult to interpret. In early experiments in macaque monkeys, lesions of V1 appeared to only partially inactivate MT (8); an additional lesion of the superior colliculus rendered MT neurons unresponsive to visual stimulation (9). Similarly, a cooling block of part of V1 failed to eliminate all visually evoked activity in the retinotopically matched portion of MT (10). In addition, functional MRI of the visual cortex in a well studied patient with V1 damage that is known for blindsight suggested that visually evoked activity in MT can be independent of V1 (11, 12). Thus, a possible source of blindsight (13), the ability to respond to visual information without awareness of the stimuli, is a relay of visual information from the superior colliculus to the pulvinar and then to extrastriate cortex (8 -10, 14).In other experiments on New World owl monkeys, MT was found to be completely dependent on V1 for visual activation, whether the lesion was recent (15) or long standing (16). In contrast, recordings from MT of the marmoset, another New World monkey, suggested that some neurons do not depend on V1 (14; for contrast, see ref. 16). These varying results suggest that species differ in dependencies of MT on V1 or that visually evoked responses in deprived parts of MT have been incorrectly attributed to an extrastriate (non-V1) source of activation.The present experiments allowed us to visualize global patterns of visual activation in MT after a block of relayed information from t...

Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area

“…Moreover, the MT isoorientation domains consisted of subdomains preferring motion in one direction and the opposite direction (17, 18). These results are similar to those described in previous studies of bush baby and owl monkey MT (17,18,24).…”

“…Moreover, the MT isoorientation domains consisted of subdomains preferring motion in one direction and the opposite direction (17, 18). These results are similar to those described in previous studies of bush baby and owl monkey MT (17,18,24).To examine whether MT neurons proportionately or disproportionately represent cardinal and oblique orientations, we mapped the amount of MT cortical space devoted to representing different orientations. Specifically, in the orientation preference maps, we examined the distributions of pixels signifying different orientations and assessed the overall relationship between preferred orientations and the amount of cortical space that represented these orientations.…”

“…It seems likely that some of the effect may be relayed from V1, which projects directly and indirectly to MT (29). In owl monkeys, lesions and deactivations of V1 rendered MT unresponsive to visual stimuli (24,38). However, reanalysis of the orientation preference maps from our previous study revealed only a small and inconsistent overrepresentation of cardinal orientations in the region of V1 representing 0-10°eccen-tricity in owl monkeys, whereas more peripheral portions of V1 were unavailable for imaging (23).…”

“…Five hemispheres were imaged in this study; three of them yielded high-quality functional maps. Some data from these animals were presented previously in abstract form,** and part of the data reported here was used for a separate analysis in an earlier paper (24).…”

“…All animals were handled according to an approved protocol from the Vanderbilt University Animal Care and Use Committee. Animals were prepared for surgery, paralyzed, and anesthetized as described elsewhere (18,23,24,39). Five hemispheres were imaged in this study; three of them yielded high-quality functional maps.…”