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Disparate substrates for head gaze following and face perception in the monkey superior temporal sulcus

  1. Karolina Marciniak  Is a corresponding author
  2. Artin Atabaki
  3. Peter W Dicke
  4. Peter Thier  Is a corresponding author
  1. Hertie Institute for Clinical Brain Research, University of Tuebingen, Germany
Research Article
Cite this article as: eLife 2014;3:e03222 doi: 10.7554/eLife.03222
4 figures

Figures

Experimental paradigm and behavioral results (‘gaze following’ paradigm).

(A) Stimuli. 16 portraits used in the gaze following and identity matching tasks, arranged by the same identity (rows) or head orientations (columns, demonstrator's head orientation eccentricity indicated in brackets). The arrows point to the correct target dot in gaze following (red) and identity matching task (green). Arrows and the scale with the eccentricity of the target as seen by the observer were not visible during the experiment. Portraits and target bar were presented on an otherwise black background (here shown as gray for better visualization). (B) Sequence of events. Exemplary gaze following (left) and identity matching (right) trials. (C) Exemplary horizontal eye movements sampled during a typical fMRI run. The gray shaded horizontal area around 0° indicates the limits (±2°) of the fixation window, the red areas indicate gaze following blocks and the green ones identity matching blocks. White areas outline the 'fixation-only' blocks. (D) Median percentages of correct answers in gaze following (red) and identity matching blocks (green), pooled separately for each observer (M1: 138 blocks; M2: 150 blocks) in ‘gaze following’ paradigm. Error bars represent 95% confidence intervals. The difference was not significant (ns, Wilcoxon signed rank test: p=0.67 [M1], p=0.43 [M2]). Dashed line indicates the chance level in each task (25%). (E) Mean reaction times in gaze following (red) and identity matching blocks (green), pooled separately for the two observers (M1:138 blocks; M2: 150 blocks) in ‘gaze following’ paradigm. Error bars represent standard errors. The difference was not significant (ns, paired samples t test: p=0.08 [M1]; p=0.22 [M2]).

https://doi.org/10.7554/eLife.03222.003
Figure 2 with 4 supplements
Control experiments.

(A) Testing for learned associations between head orientation and the spatial position of the target. Sequence of normal gaze following trials (I) with catch trials (II) where demonstrator portrait was shifted horizontally (here by 10°). Subject's responses in the catch trials were later classified into three categories (III): (1) The 'gaze following' category (red outline). (2) The 'learned spatial association' category (blue outline). (3) The 'other' category (gray outline). Dashed lines in the figures indicate the observer’s eye gaze. (B) Testing for associations between head orientation and the ordinal position of targets. Sequence of normal gaze following trials (I) with catch trials (II) where the 10° eccentricity targets maintained their standard spatial position but changed their ordinal position (II). The responses in catch trials were later classified into three categories (III): (1) The 'gaze following' category (red outline). (2) The 'learned order association' category (blue outline). (3) The 'other' category (gray outline). (C) The results of control Experiment 1 (Figure 2A). Mean percentages of responses classified as the 'gaze following' category (red column), the 'learned spatial associations' category (blue column) and in the 'other' category (gray column). Both monkeys showed significantly more responses in the 'gaze following' category than in the two other ones (repeated measures 1-way ANOVA, significant effect of the factor 'response category' (F2,54 = 51.23, p<0.001 [M1]; F2,32 = 127.4, p<0.001 [M2]). (D) The results of the control Experiment 2 (Figure 2B). Mean percentages of responses classified as the 'gaze following' category (red column), the 'learned order associations' category (blue column) and in the 'other' category (gray column). Both monkeys showed significantly more responses in the 'gaze following' category than in the two other ones (repeated measures 1-way ANOVA, significant effect of the factor 'response category' [F2,20 = 47.8, p=0.001 (M1); F2,22 = 132.2, p<0.001 (M2)]); In [C] and [D] post hoc pairwise comparisons [with Bonferroni correction] are indicated with significance levels: ***p<0.001, **p<0.01, *p<0.05, not significant [ns]; n indicates the number of experimental repetitions. Error bars represent standard errors. M1 = monkey 1, M2 = monkey 2.

https://doi.org/10.7554/eLife.03222.004
Figure 2—figure supplement 1
Design of the control experiments testing for learned associations between facial identity and the spatial position of the target.

It was performed outside the MRI scanner in order to shed light on the strategies utilized to solve the identity matching task. The observer was confronted with a sequence of normal identity matching trials (I) with occasional catch trials (II, 6–12% share) in which the demonstrator portrait was shifted horizontally (shifts of −10°, −5°, 5° and 10° with respect to the default central position, the cartoon assumes −5° shift). In any case, the observer was asked to generate a saccade towards the target singled out by facial identity. In the case of ordinary identity matching trials the observer was rewarded contingent on the response. In the case of catch trials, a reward was granted on 50% of the catch trials, independent of the target chosen, provided the observer had stayed on the chosen target for at least 1 s. These responses were later classified into three strategy categories (III). (1) The 'learned absolute spatial associations' category (blue outline): target chosen according to its absolute spatial position associated with a given demonstrator facial identity, (invariant in space after demonstrator's portrait shift). (2) The 'learned relative spatial associations' category (red outline): target chosen according to its relative distance associated with a given demonstrator portrait's identity (now shifted horizontally together with the demonstrator portrait; the cartoon assumes a shift of the target from 10° to 5°). (3) The 'other' category (gray outline). Dashed lines in the figures indicate the observer's eye gaze.

https://doi.org/10.7554/eLife.03222.005
Figure 2—figure supplement 2
Design of the control experiment testing for associations between the facial identity and the ordinal position of targets.

Again it was performed outside the MRI scanner in order to shed light on the strategies utilized to solve the identity matching task. Also here the observer was confronted with a sequence of normal identity matching trials (I) with occasional catch trials (II, 6–12% share). In catch trials the outer targets stayed in their standard locations of −10° and 10° respectively, whereas inner targets (normally at −5° and 5° respectively) were shifted further out to −15° and 15° eccentricity respectively. As a consequence of this shift, the 10° eccentricity targets maintained their standard spatial position but changed their ordinal position (from 1 and 4 to 2 and 3) (II). Again, the responses in catch trials later classified into three categories (III): (1) The 'learned order associations' strategy (target chosen according to its ordinal position in the target order with respect to a given demonstrator's identity, shifted from 10° to 15° on the cartoon, blue outline). (2) The 'learned absolute spatial associations' category (target chosen according to its absolute spatial position associated with a given demonstrator's identity, keeping his position at 10° on the cartoon, red outline), (3) The 'other' strategy.

https://doi.org/10.7554/eLife.03222.006
Figure 2—figure supplement 3
The results of the control experiment testing for associations between demonstrator's identity and target location (Figure 2—figure supplement 1).

Mean percentages of responses classified as falling into the 'learned absolute spatial associations' category (blue column), the 'learned relative spatial associations' category (red column) and in the 'other' category (gray column). Both monkeys exhibited significantly more responses in the 'learned absolute spatial associations' category than in the two other categories (repeated measures 1-way ANOVA, significant effect of the factor 'response category' [F2,18 = 30.6, p<0.001 (M1); F2,18 = 104.2; p<0.001 (M2)]; post hoc pairwise comparisons [with Bonferroni correction] are presented on the graph with their significance levels: ***p<0.001, **p<0.01, *p<0.05, not significant [ns]; n indicates the number of experimental repetitions). Error bars represent standard errors.

https://doi.org/10.7554/eLife.03222.007
Figure 2—figure supplement 4
The results of the control experiment testing for associations between demonstrator's identity and the ordinal position of targets (Figure 2—figure supplement 2).

Mean percentages of responses classified as falling in the 'learned order associations' category (blue column), the 'learned absolute spatial associations' category (red column), and the 'other' category (gray column). We found differences in the preferred categories between two observers (repeated measures one-way ANOVA [F2,18 = 170.9, p<0.001 (M1); F2,22 = 175.9, p=0.01 (M2)], post hoc pairwise comparisons [with Bonferroni correction] are presented on the graph with their significance levels: *p<0.05, **p<0.01, ***p<0.001, not significant [ns]. n indicates the number of experimental repetitions). Error bars represent standard errors. M1 = monkey 1, M2 = monkey 2.

https://doi.org/10.7554/eLife.03222.008
Figure 3 with 1 supplement
'Gaze following vs identity matching' BOLD contrast.

(A) Lateral views of the partially inflated hemispheres of monkeys M1 and M2 with significant (p<0.005, uncorrected, 5 contiguous voxels) BOLD 'gaze following vs identity matching' contrasts. A = anterior, P = posterior, L = left, R = right, sts = superior temporal sulcus, ios = inferior occipital sulcus, lus = lunate sulcus, ls = lateral sulcus. (B) Coronal sections through the brains of monkeys M1 and M2 with corresponding significant BOLD contrast from (A). The color scale bar gives the t-scores indicating the size of significant BOLD contrasts. The numbers in the left corners of each section indicate the distance from the vertical interaural plane of each monkey. L = left, R = right.

https://doi.org/10.7554/eLife.03222.009
Figure 3—figure supplement 1
'Gaze following vs identity matching' BOLD contrast evoked in Experiment 1 using a unilateral small coil placed on the left hemisphere of M1.

Coronal sections based on T1 weighted anatomical scans cut through the brain M1 with significant BOLD responses mapped onto the sections. (A) Absence of significant activity at a significance level p<0.005, uncorrected, 5 contiguous voxel. (B) Significance level p<0.05, uncorrected, 5 contiguous voxels. The numbers in the left corner of each section indicate the AP-distance from interaural plane of the monkey. Notice that the BOLD response is contralateral to the position of the coil. L = left, R = right.

https://doi.org/10.7554/eLife.03222.010
Figure 4 with 1 supplement
Comparison of the patterns of BOLD responses to 'gaze following' and 'identity matching' with the face patch BOLD pattern, delineated by the passive viewing of faces.

(A) Lateral views of the partially inflated hemispheres of monkeys M1 and M2 with borders of significant BOLD responses. Face patches (orange) based on 'faces vs nonfaces' contrast (p<0.05, uncorrected, 5 contiguous voxels) masked with an 'all non-scrambled vs all scrambled' objects' contrast (p<0.05 uncorrected). The red contours: significant BOLD contrasts for the 'gaze following vs identity matching' comparison (p<0.005, uncorrected, 5 contiguous voxels). The green contours: significant BOLD contrasts for the opposite, 'identity matching vs gaze following' comparison (p<0.05, uncorrected, 5 contiguous voxels). A = anterior, P = posterior, L = left, R = right, sts = superior temporal sulcus, ios = inferior occipital sulcus, lus = lunate sulcus, ls = lateral sulcus. (B) Coronal sections through the brains of monkeys M1 and M2 with corresponding significant BOLD contrasts from (A). The numbers in the left corners indicate the distance from the vertical interaural plane of each monkey (positive values anterior, neg. posterior) (L = left, R = right).

https://doi.org/10.7554/eLife.03222.011
Figure 4—figure supplement 1
Examples of stimuli used in the 'passive face perception' experiment.

(A) Biological and non-biological objects, (B) faces and scrambled versions of objects/ faces (lowermost row), (C) grid-scrambled images. The human faces were taken from the Nottingham Scans database (free for research use under the terms of a Creative Commons Attribution license, http://pics.psych.stir.ac.uk), all other images were from a variety of freely available sources.

https://doi.org/10.7554/eLife.03222.012

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