Distributed and Dynamic Neural Encoding of Multiple Motion Directions of Transparently Moving Stimuli in Cortical Area MT

Model fits of the response tuning curves elicited by bidirectional stimuli separated by 60°. A, PV accounted for by the LWS and the SNL model. B, Weights for the component responses obtained using the SNL model fit. Each dot in A and B represents data from one neuron. Colored dots in B indicate that the two response weights are significantly different. C, Distribution of the response weight for each stimulus component. D–F, Direction tuning curves and their model fits of three example neurons. These neurons are the same as those shown in Figure 1B–D.

Population-averaged tuning curves elicited by bidirectional stimuli separated by 60° and by constituent unidirectional components. A, Tuning curves averaged across all neurons in the sample. B, Averaged across neurons that showed a single response peak and no side bias to the bidirectional stimuli. C, Neurons that showed side bias toward the stimulus component at the C-side of the two component directions (i.e., Dir. 2). D, Neurons that showed side bias toward the CC-side component (i.e., Dir. 1). E, Neurons that showed two response peaks. The convention of the abscissa is the same as that in Figure 1. Abscissas for component Dir. 1 and Dir. 2 are not plotted for simplicity. The width of each curve indicates SE.

Consistent side bias of response tuning curves across different angular separations. A, Averaged response tuning-curves across 18 neurons that showed side bias to the C-side component of the bidirectional stimuli separated by 60°. B, Averaged response tuning curves across 26 neurons that showed side bias to the CC-side component of the bidirectional stimuli separated by 60°. The width of each curve indicates SE. C, Response weights obtained using the SNL model fit for the combined 44 neurons that showed side bias to the bidirectional stimuli separated by 60°. The “biased-side” in the ordinate was determined by the response to 60° DS. Each dot represents data from one neuron. Solid dots indicate that the response weight for one stimulus component was significantly greater than the other component (permutation test, p < 0.05). The mean weight for the component response to the “biased-side” defined at 60° DS was significantly greater than the weight to the other stimulus component at angular separations of 45°, 90° and 135°. p-values are the results of one-tailed paired t test. A1–C1, 45° DS; A2–C2, 60° DS; A3–C3, 90° DS; A4–C4, 135° DS. Note that we allowed the side-biased neurons to have either a single response peak or two response peaks in this analysis.

Relationship between the shapes of response tuning curves to bidirectional and unidirectional stimuli. The results were from 79 neurons that showed side bias in their tuning curves to the bidirectional stimuli separated by 60°. A, Relationship between the peak locations of the response tuning to the bidirectional stimuli R₁₂ and the average of the responses elicited by individual stimulus components R_avg = (R₁ + R₂)/2. The peak location is represented as the VA direction of the bidirectional stimuli. B1, Relationship between the difference of the response weights for the two stimulus components obtained from the SNL model fit of R₁₂ and the skewness of the unidirectional tuning curve (see Materials and Methods). w₂ and w₁ correspond to the response weights for Dir. 2 and Dir. 1, respectively (Fig. 1 diagram). B2–B4, Response tuning curves to the unidirectional stimuli of three neurons that had negative (B2), near zero (B3), and positive skewness (B4). These neurons are marked in B1 using the corresponding colors. The neuron shown in B3 is the same example neuron shown in Figure 1B.

Time course of response tuning to bidirectional stimuli separated by 60°. A–D, Responses of neurons showing side bias to bidirectional stimuli. E–H, Responses of neurons showing two peaks to bidirectional stimuli. A, E, Subpopulation-averaged response tuning curves to bidirectional stimuli at different time epochs after the stimulus motion onset. The duration of each time epoch is 50 ms. The tuning curves of later epochs are stacked on earlier ones. The number in figure legends indicates the middle point of each time epoch. B, F, Time course of the subpopulation-averaged response tuning to bidirectional stimuli (i.e., R₁₂). Ordinates indicate the middle point of each time epoch. C, G, Time course of the average of the component responses (i.e., R_avg), averaged across neurons in each subpopulation. D, H, Difference between the response to bidirectional stimuli shown in B and F and the average of the component responses shown in C and G, respectively. In A–C, we pooled the results from neurons that showed side bias to the component directions at the C-side (i.e., Dir. 2) and CC-side (i.e., Dir. 1) together by first flipping the bidirectional and unidirectional tuning curves of neurons that showed the side bias to Dir. 2 along the axis of VA direction 0°. The white and gray horizontal lines in B–D and F–H indicate the neuronal response onset to the stimulus motion. In D and H, the deviation from the average of the component responses emerged later than the neuronal response onset.

The temporal evolution of the response peak(s) in the tuning curve to bidirectional stimuli separated by 60°. A, Location and amplitude of the response peak of neurons that showed a single peak and side bias. We pooled neurons that showed side bias to the C-side (i.e., Dir. 2) and CC-side (i.e., Dir. 1) together as in Figure 6, A and B. B, Peak locations and amplitudes of neurons that showed two response peaks to bidirectional stimuli. Right side and left side refer to the peaks seen in Figure 6, E and F. The peak location and magnitude were calculated based on averaged response tuning curves across neurons in each subgroup. The tuning curve was calculated within a 50 ms time epoch, sliding at a 10 ms step. Abscissa indicates the middle point of each time epoch.

Temporal development of side bias in the response tuning curves elicited by bidirectional stimuli at different angular separations. A1–A3, Responses elicited by bidirectional stimuli separated by 45°. B1–B3, 60° DS. C1–C3, 90° DS. D1–D3, 135° DS. A1–D1, Subpopulation-averaged tuning curves of responses at different time epochs elicited by bidirectional stimuli. The duration of each time epoch is 50 ms. A2–D2, Time course of the response tuning to bidirectional stimuli averaged across side-biased neurons at each DS. Classification for the side-biased neurons was based on the responses to the bidirectional stimuli at each DS. A3–D3, Time course of the average of the component responses. Conventions are the same as for Figure 6, A–C. The results from neurons that showed side bias to the component directions at the C-side and CC-side were pooled together. This analysis included side-biased neurons that showed either a single response peak or two peaks at each DS.

Illustration of two perceptual discrimination tasks. A, In Task I, a bidirectional stimulus and a unidirectional stimulus were presented simultaneously. The animal was required to make a saccadic eye movement after the stimulus offset toward the location where a bidirectional stimulus was presented. The stimulus centered on the RF was either bidirectional or unidirectional. B, In Task II, only one stimulus, either bidirectional or unidirectional, was presented in a given trial and centered on the RF. The animal was required to make a saccadic eye movement after the stimulus offset toward one reporting target if the stimulus was bidirectional or the other target if the stimulus was unidirectional.

Direction tuning curves obtained while the animals performed the perceptual discrimination tasks. The DS of the bidirectional stimuli was 60°. A1–C1, Three example neurons recorded while monkey GE performed Task I. A2–C2, Three example neurons recorded while monkey BJ performed Task II. A3–C3, Direction tuning curves averaged across subpopulations of neurons from the two animals. A, Neurons showing side bias to the CC-side. B, Neurons showing side bias to the C-side. C, Neurons showing two separate peaks in the response tuning curves.

Time course of the direction tuning curves obtained while an animal performed a perceptual discrimination task. The DS of the bidirectional stimuli was 60°. Results were recorded while monkey BJ performed Task II, during which the onset of visual motion was separated from the stimulus onset (see Materials and Methods). A, B, Averaged responses from 25 neurons that showed side bias to the bidirectional stimuli. C, D, Averaged responses from 14 neurons that showed two peaks in the tuning curves to the bidirectional stimuli. A, C, Response tuning curves to the bidirectional stimuli. Ordinates indicate the middle point of each time epoch of 50 ms. B, D, Average of the component responses.

Stimulus discrimination using a classifier of support vector machine (SVM). A–C, Procedure of constructing a “single-trial population neural response” based on the direction tuning curve. D–F, Discrimination performance of the classifier. A, Trial-by-trial tuning curves of one example neuron in response to the bidirectional stimuli of 60° DS. A tuning curve based on one block of trials (red) was picked. B, The picked single-trial tuning curve from A (red) was duplicated and shifted in a step of 7.5° to create the tuning curves of 48 “cloned” neurons. For clarity, only the cloned neurons that had PDs in a step of 30° are shown (black). C, Single-trial population neural response of the cloned neurons elicited by a bidirectional stimulus moving at VA direction 0°. D, Discrimination between the bidirectional stimuli of 60° DS and the unidirectional stimulus moving at the same VA direction. Stimulus classification was based on the neural responses of all neurons in the dataset (black) or one of three subgroups of neurons (green, blue, and red). The label “sub” in the abscissa means a subset of randomly selected neurons within the groups of averaging and side-biased neurons. E, Discrimination between a bidirectional stimulus of 60° DS and another bidirectional stimulus that had a DS of 45°, 90°, and 135°, respectively, and moving at the same VA direction. When discriminating between DS 60° and 90°, the performances of the side-biased neurons and the averaging neurons were nearly identical. In this analysis, the side-biased neurons only contained a single response peak to the bidirectional stimulus of 60° DS, so the side-biased and two-peaked neuron populations did not overlap. F, Discrimination between a unidirectional and a bidirectional stimulus. The classifications of averaging, side-biased, and two-peaked neurons were based on the responses to DS 60°.

Z-transformed pattern and component correlation between the responses elicited by 135° plaid and pattern/component predictions. Each dot represents results from one neuron. A, Results from overall neuron population. B, Results from neurons approximately followed the average of the component responses when responding to the bidirectional random-dot stimuli that had a DS of 60°. C, Neurons with responses to the random-dot stimuli that showed side bias. D, Neurons with responses to the random-dot stimuli that showed two response peaks.