Fine discrimination training alters the causal contribution of macaque area MT to depth perception

Abstract

When a new perceptual task is learned, plasticity occurs in the brain to mediate improvements in performance with training. How do these changes affect the neural substrates of previously learned tasks? We addressed this question by examining the effect of fine discrimination training on the causal contribution of area MT to coarse depth discrimination. When monkeys are trained to discriminate between two coarse absolute disparities (near versus far) embedded in noise, reversible inactivation of area MT devastates performance. In contrast, after animals are trained to discriminate fine differences in relative disparity, MT inactivation no longer impairs coarse depth discrimination. This effect does not result from changes in the disparity tuning of MT neurons, suggesting plasticity in the flow of disparity signals to decision circuitry. These findings show that the contribution of particular brain area to task performance can change dramatically as a result of learning new tasks.

Figure 1

Schematic illustration of the three discrimination tasks. Upper panels show a top-down view of the stimulus geometry; lower panels show a front view. a) The coarse depth task. In each trial, 'signal' dots appeared at one of two disparities (±0.5°), either near or far relative to the plane of fixation (short horizontal line segments), and the monkey reported whether the net depth was near or far. Here, the stimulus consists of 50% signal dots and 50% noise dots. Filled and open dots represent the left and right half images, respectively. b) The fine depth task. The stimulus is a bi-partite random-dot stereogram in a center/surround configuration. The disparity of the surround was fixed at either +0.2° or −0.2°, and the disparity of the center patch varied in fine steps around this value. Monkeys reported whether the center patch was in front of or behind the surround patch. c) The direction discrimination task. 'Signal' dots (filled) moved either rightward or leftward, and the monkey reported the direction of global motion. Here, the stimulus consists of 50% signal dots and 50% noise dots (50% coherence).

Figure 2

Data from a representative experiment performed on monkey Bk prior to learning the fine depth task. Each panel shows the proportion of correct responses as a function of stimulus strength. Black data points show psychophysical performance prior to inactivation ('Pre'). Cyan data show performance within an hour following inactivation ('+40 min' or ‘+45min’), and red data show performance on the following morning ('+1d'). Green data show performance two days after injection ('+2d'). Smooth curves are the best fits of a Weibull function. a) Effects of inactivation on the coarse depth task. b) Effects of inactivation on the direction discrimination task.

Figure 3

Summary of inactivation effects on coarse depth (a, c) and direction discrimination (b, d) prior to fine depth training. Each panel shows psychophysical thresholds at three time points: prior to muscimol injection ('Pre'), the day following injection ('+1d'), and two days after inactivation ('+2d'). Each colored curve represents data from a single experiment, and data of the same color in a and b come from the same experiment (also true for c and d). Error bars show the 95% confidence interval for each threshold measurement. Note that thresholds were not allowed to exceed 100% in the curve fitting procedure. a, b) data from monkey Bk. c, d) data from monkey J.

Figure 4

Effects of stimulus location on behavioral deficits resulting from MT inactivation. Each row shows data from one experiment. Hatched bars show psychophysical thresholds on the day following muscimol injection ('+1d'); filled bars show thresholds following recovery ('+2d'). Each pair of hatched and filled bars corresponds to a stimulus location as diagrammed on the right (HM: horizontal meridian; VM: vertical meridian). a, d) Data from a direction discrimination experiment. Following inactivation (hatched bars), psychophysical threshold was significantly elevated at the location of the receptive field (gray circle), modestly elevated at locations 1 and 3, and unaffected at locations 2 and 4. b, e) Data from a coarse depth discrimination experiment, showing threshold elevation only at the location of the receptive field. c, f) Data from an additional direction discrimination experiment, showing a similar pattern of results.

Figure 5

Data from a representative experiment performed after monkey Bk learned the fine depth task. The effect of inactivation was tested on all three discrimination tasks: fine depth (a), coarse depth (b), and direction (c). Data are shown in the format of Fig. 2.

Figure 6

Summary of results from all experiments performed on monkey Bk (top row) and monkey R (bottom row) after fine depth training. Results are shown for the fine depth (a, d), coarse depth (b, e), and direction (c, f) tasks. The format of each panel is identical to that of Fig. 3.

Figure 7

Summary of disparity tuning properties of single MT neurons before and after fine depth training. The left column shows pooled data from two animals (monkeys Bn and Jr, filled bars) before fine depth training, and data from two animals (monkeys Bn and R, hatched bars) after fine depth training. The right column shows data from monkey Bn, who contributed to both training groups. a, b) Distributions of the disparity discrimination index (DDI), a measure of tuning strength. c, d) Distributions of disparity frequency, a measure of tuning width. e, f) Distributions of the disparity at which each neuron shows its peak response (or trough response for tuned-inhibitory neurons).