The Journal of Neurophysiology Vol. 84 No. 5 November 2000, pp. 2658-2669
Copyright ©2000 by the American Physiological Society

Center-Surround Interactions in the Middle Temporal Visual Area of the Owl Monkey

Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115-5701

Born, Richard T. Center-Surround Interactions in the Middle Temporal Visual Area of the Owl Monkey. J. Neurophysiol. 84: 2658-2669, 2000. Microelectrode recording and 2-deoxyglucose (2dg) labeling were used to investigate center-surround interactions in the middle temporal visual area (MT) of the owl monkey. These techniques revealed columnar groups of neurons whose receptive fields had opposite types of center-surround interaction with respect to moving visual stimuli. In one type of column, neurons responded well to objects such as a single bar or spot but poorly to large textured stimuli such as random dots. This was often due to the fact that the receptive fields had antagonistic surrounds: surround motion in the same direction as that preferred by the center suppressed responses, thus rendering these neurons unresponsive to wide-field motion. In the second set of complementary, interdigitated columns, neuronal receptive fields had reinforcing surrounds and responded optimally to wide-field motion. This functional organization could not be accounted for by systematic differences in binocular disparity. Within both column types, neurons whose receptive fields exhibited center-surround interactions were found less frequently in the input layers compared with the other layers. Additional tests were done on single units to examine the nature of the center-surround interactions. The direction tuning of the surround was broader than that of the center, and the preferred direction, with respect to that of the center, tended to be either in the same or opposite direction and only rarely in orthogonal directions. Surround motion at various velocities modulated the overall responsiveness to centrally placed moving stimuli, but it did not produce shifts in the peaks of the center's tuning curves for either direction or speed. In layers 3B and 5 of the local motion processing columns, a number of neurons responded only to local motion contrast but did so over a region of the visual field that was much larger than the optimal stimulus size. The central feature of this receptive field type was the generalization of surround antagonism over retinotopic spacea property similar to other "complex" receptive fields described previously. The columnar organization of different types of center-surround interactions may reflect the initial segregation of visual motion information into wide-field and local motion contrast systems that serve complementary functions in visual motion processing. Such segregation appears to occur at later stages of the macaque motion processing stream, in the medial superior temporal area (MST), and has also been described in invertebrate visual systems where it appears to be involved in the important function of distinguishing background motion from object motion.