Columnar organization of directionally selective cells in visual area MT of the macaque

Abstract

We recorded from single neurons in visual area MT of the macaque in order to examine the spatial distribution of its directionally selective cells. The animals were paralyzed and anesthetized with nitrous oxide. All MT neurons (n = 614) responded better to moving stimuli than to stationary stimuli. For 55% of the neurons, responses to moving stimuli were independent of stimulus color, shape, length, or orientation. For the remaining cells, stimulus length affected the response magnitude and tuning bandwidth but not the preferred direction. MT neurons were divided into four categories on the basis of their sensitivity to moving stimuli: 60% responded exclusively to one direction of motion, 24% responded best to one direction with a weaker response in the opposite direction, 8% responded equally well to two opposite directions of motion, and 8% responded equally well to all directions of motion. The direction preferences of successively sampled cells on a penetration either changed by small increments or occasionally by approximately 180 degrees. Thus, there is a systematic representation of direction of motion. The representation of axis of motion, i.e., the orientation of the path along which a stimulus moves, is more continuous than the representation of direction of motion. There was a systematic relationship between penetration angle and rate of change of preferred axis of motion, indicating that cells with a similar axis of motion preference are arranged in vertical columns. Furthermore, axis of motion columns appear to exist in the form of continuous slabs in area MT. The size of these slabs is such that 180 degrees of axis of motion are represented in 400-500 micron of cortex. There was also a systematic relationship between penetration angle and frequency of 180 degrees reversals, indicating that cells with a similar direction of motion preference are also organized in vertical columns and cells with opposite direction preferences are located in adjacent columns within a single axis of motion column. Just as in macaque striate cortex where approximately 500 micron of cortex contain the mechanism for the local analysis of stimulus orientation, so in MT approximately 500 micron of cortex contain the mechanism for the local analysis of stimulus motion.

Two-dimensional map of direction selectivity in cortical visual area MT of Cebus monkey

“…This type of "sequence regularity" closely matches that seen along single electrode penetrations in macaque MT (Albright et al 1984). As shown in Figure 2, the second array penetration (P2) happened to traverse a region of area MT that was also mapped by P1.…”

“…As previously pointed out by Albright et al (1984), the preferred direction maps reveal that gradual sequences of preferred axis of motion are commonly interspersed with 180 • reversals in preferred direction of motion. Adjacent recording sites that exhibit such 180 • directional discontinuities disappear in Figure 4.…”

“…Otherwise, the closer the electrode track is to the center of the pinwheel, larger the rate of change of axis of motion per unit of distance traveled. Both in own data, as well as in Albright et al (1984) data, the plot of axis of motion in degrees vs. distance consist of sigmoid segments, either ascending (clockwise rotation) or descending (counterclockwise ones) on the ordinate representing axis of motion. When two consecutive ascending (or descending) sigmoid segments appear in a penetration they are separated by a fracture or a jump in the plot.…”

“…These maps were derived from 108 "hand-mapped" measures of directional preference at each recording site along three multielectrode penetrations made in Case 2. Visualization of ordered columnar arrangements in area MT was often facilitated by examining preferred axis of motion, rather than preferred direction of motion, because abrupt directional reversals disappears in this type of representation (see Albright et al 1984). Figure 3 contains two direction-of-motion maps obtained from area MT in Case 2.…”

The complementary brain: unifying brain dynamics and modularity

“…An object can contain contours of many different orientations which all move in the same direction as part of the object's motion. Both psychophysical and neurophysiological experiments have shown that the motion stream pools information from many orientations that are moving in the same direction to generate precise estimates of a moving object's direction and speed [19][20][21][27][28][29] . Lesions of the form system also show that, on its own, the motion system can make only coarse depth estimates 30,31 .…”