Attention reshapes center-surround receptive field structure in macaque cortical area MT

Abstract

Directing spatial attention to a location inside the classical receptive field (cRF) of a neuron in macaque medial temporal area (MT) shifts the center of the cRF toward the attended location. Here we investigate the influence of spatial attention on the profile of the inhibitory surround present in many MT neurons. Two monkeys attended to the fixation point or to 1 of 2 random dot patterns (RDPs) placed inside or next to the cRF, whereas a third RDP (the probe) was briefly presented in quick succession across the cRF and surround. The probe presentation responses were used to compute a map of the excitatory receptive field and its inhibitory surround. Attention systematically reshapes the receptive field profile, independently shifting both center and surround toward the attended location. Furthermore, cRF size is changed as a function of relative distance to the attentional focus: attention inside the cRF shrinks it, whereas directing attention next to the cRF expands it. In addition, we find systematic changes in surround inhibition and cRF amplitude. This nonmultiplicative push-pull modulation of the receptive field's center-surround structure optimizes processing at and near the attentional focus to strengthen the representation of the attended stimulus while reducing influences from distractors.

Figure 1.

Attention task and stimulus arrangement. (A) The trial started with fixation of the yellow fixation point. A stationary RDP, shown for 440 ms, cued the later target position. After a delay of 133 ms, target and distractor RDPs appeared, moving in the antipreferred direction. After another 173 ms, the mapping of the receptive field with the probe started. The probe RDP, moving in the preferred direction, was presented in random order at ∼80 positions for 187 ms each, separated by 27 ms. The monkey was rewarded for detecting a brief (133 ms) direction change of the target, which could occur between 253 and 6000 ms after target and distractor onset. (B) Target (black circle filled white) and distractor (white circle filled black) were presented in or next to the estimated receptive field center at equal eccentricity from the fixation point. The probe grid (light gray dots) spanned the receptive field center (red/yellow) and surround (blue) and was arranged so that either 1 or 2 probe positions fell onto the receptive field center, between the target and distractor RDPs. The illustration shows an ideal case were the full surround extent could be measured; often, the surround was larger than the mapped area. Drawings are not to scale.

Figure 2.

Center and surround shift for 2 example cells. (A, C) Receptive field maps for 2 example cells when attention was either on the left or on the right target (black circle filled white). Maps were rotated for convenience so that the fixation point (white square filled black) was up. The contour lines mark the quarter-height level of excitatory/inhibitory modulation at which center and surround were cut for the centroid analysis (white: center, gray: surround). The vertical lines show the volume centroids (white: center, gray: surround) along the target–distractor axis, calculated over the outlined area. For both cells, center and surround profiles shift toward the attended stimulus. (B, D) Difference maps for the same 2 cells were created by subtracting the probe responses with attention left from those with attention right. Regions of positive response differences (i.e., stronger response with attention right) are shown in red/yellow, whereas negative response differences are shown in blue/cyan. Contour lines mark the 5% level of the cRF for attention left (black contour) and attention right (white contour). The gray dots show the probe positions that were used to calculate the mean response differences left and right of both centers (see Methods for details). For both cells, the response differences are more positive on the left than on the right of the cRF, meaning that surround inhibition is weaker on the unattended side and stronger on the attended side.

Figure 3.

Distribution of center and surround shifts relative to the cRF diameter. (A) The histogram shows a significant shift of the cRF center toward the attended stimulus by 10.1% (±1% SEM, P < 0.0005, n = 100) of the cRF diameter (monkey D [green]: 8.7%, ± 1.2%, P < 0.0005, n = 58; monkey T [red]: 12.1%, ± 1.5%, P < 0.0005, n = 42). (B) The histogram shows a significant shift of the surround toward the attended stimulus by 20.2% (±7.7% SEM, P = 0.022, n = 45 cells in the surround centroid analysis) of the cRF diameter (monkey D: not significant, P = 0.182, n = 26; monkey T: 22.3%, ± 9.4%, P = 0.043, n = 19). Triangles mark the mean shift magnitudes (gray: overall, green: monkey D, red: monkey T).

Figure 4.

Hypothetical difference map. Hypothetical difference maps were created by subtracting 2 receptive field maps, each simulated by the difference of a narrow and peaked 2D-Gaussian (the receptive field center) and a spatially overlapping broad and flat 2D-Gaussian (the receptive field surround). (A) Only the cRF is shifted between both conditions. Here, a leftward shift of the receptive field center was subtracted from a rightward shift, resulting in a peak of positive response differences on the right and a dip of negative response differences on the left. (B) Attention additionally shifts the surround, resulting in an additional peak of positive response differences on the left and an additional dip of negative response differences on the right along the shift axis. See supplementary materials for further examples, formulas and choice of parameters.

Figure 5.

Distribution of the bias in mean response difference in the difference map analysis. The histogram shows a significant bias in mean response difference left and right of the cRF, so that the mean response difference is more positive on the left than on the right (mean 0.6 Hz ± 0.2 Hz SEM, gray triangle, P = 0.013, n = 58 surround cells), corresponding to weaker surround inhibition on the unattended side and stronger surround inhibition on the attended side. Both monkeys analyzed separately show the same trend (monkey D [green]: mean 0.6 Hz ± 0.3 Hz, P = 0.092, n = 34; monkey T [red]: mean 0.6 Hz ± 0.3 Hz, P = 0.067, n = 24).

Figure 6.

Size changes of the receptive field center with attention. (A) Receptive field maps of an example cell when a task was done at the fixation point (left graph, white filled square) and when a position inside the cRF was attended (right graph, black circle filled white). The cRF area, outlined in white, is clearly reduced with attention inside the cRF. (B) Plots the distribution of cRF size changes (in % of the cRF diameter in the fixation condition) for all 142 cases in which attention was directed into the cRF. There is a significant shrinkage of 4.7% (±1.3% SEM, P < 0.0005; monkey D: 5.6%, ± 1.8%, P = 0.011, n = 77; monkey T: 3.6%, ±1.7%, P = 0.002, n = 65). (C) Receptive field maps of another example cell are compared for the fixation task (left graph) and attending to a spot next to the cRF (outside of the quarter-height defined excitatory region; right graph). Here, the cRF area grows with attention. (D) Plots the distribution of cRF size changes for all 58 cases in which attention was directed to the border of the cRF. There is a significant expansion of 14.2% (±4.6% SEM, P = 0.002; monkey D: 20.8%, ±6.4%, P < 0.0005, n = 39; monkey T: not significant, P = 0.717, n = 19).

Figure 7.

Receptive field size change as a function of the distance of the attentional target to the receptive field center. For the 200 attention–fixation pairs, the change in cRF diameter is plotted as a function of the distance between target and cRF center, which was normalized to the cRF radius so that a distance of 1 approximately marks the cutoff between attention inside and attention next to the cRF. Arrows mark data points that fall beyond the axis limits, numbers indicate how many data points are represented by each arrow. The correlation between size change and target-center distance is significant (r = 0.4, P < 0.0005; monkey D: r = 0.46, P < 0.0005, n = 116; monkey T: r = 0.34, P = 0.002, n = 84).

Figure 8.

A mechanism for a feedforward surround shift. (A) Spatial tuning profiles (response as a function of position) of 2 V1 receptive fields with inhibitory surrounds are represented by the difference of 2 Gaussians. (B) Their additive combination results in a broader spatial tuning curve, with inhibitory surround, representing the receptive field of an MT neuron. (C and D) The same receptive fields are shown with attention selectively increasing the gain of that V1 receptive field closer to the attentional focus (marked by the red arrow): multiplicative gain modulation of one of the V1 receptive fields (C) shifts the peak of the MT receptive field toward the direction of spatial attention, and at the same time increases surround strength on the same side (D).