Recent evidence suggests that preverbal infants' gaze following can be triggered only if an actor's head turn is preceded by the expression of communicative intent []. Such connectedness between ostensive and referential signals may be uniquely human, enabling infants to effectively respond to referential communication directed to them. In the light of increasing evidence of dogs' social communicative skills [], an intriguing question is whether dogs' responsiveness to human directional gestures [] is associated with the situational context in an infant-like manner. Borrowing a method used in infant studies [], dogs watched video presentations of a human actor turning toward one of two objects, and their eye-gaze patterns were recorded with an eye tracker. Results show a higher tendency of gaze following in dogs when the human's head turning was preceded by the expression of communicative intent (direct gaze, addressing). This is the first evidence to show that (1) eye-tracking techniques can be used for studying dogs' social skills and (2) the exploitation of human gaze cues depends on the communicatively relevant pattern of ostensive and referential signals in dogs. Our findings give further support to the existence of a functionally infant-analog social competence in this species.

Results

2 Topál J.

Miklósi Á.

Gácsi M.

Dóka A.

Pongrácz P.

Kubinyi E.

Virányi Z.

Csányi V. The dog as a model for understanding human social behavior. Figure 1 Selected Frames from the Stimuli in the Ostensive and Nonostensive Conditions Show full caption Each trial presented video recordings that started with an introductory phase during which the model that had two pots on each side was facing down in a still position for 2 s (A). The second phase was an addressing phase that lasted for 3 s and differed according to the experimental conditions. In the O (ostensive; A, B, D) condition, the model raised her head, looked straight at the dog, and addressed the subject (“Hi dog!”) in a high-pitched voice (B). In the NO (nonostensive; A, C, D) condition, with her head facing down, the model addressed the dog using low-pitched voice (“Hi dog!”) while a salient moving image was overlaid on the head (C). This attention-getter was present for 2 s and served to create attentional demand similar to that in the ostensive condition. The verbal signal in the two conditions had similar duration and intensity but differed in pitch. In the cueing phase (6 s), the model turned her head toward one of the two containers (1 s) and remained motionless (5 s) while showing neutral facial expression (D). GC indicates the gaze congruent and GIC the gaze-incongruent regions of interest (ROI). Although recent research has provided important evidence about dogs' social communicative skills [], it is still unclear whether dogs' gaze following is tuned to cues that signal the human's communicative intent (e.g., eye contact, verbal addressing). In order to investigate this first, we have collected eye-gaze data from 16 adult, task-naive pet dogs. Subjects were presented with a series of movies in which a human female turned her attention toward one of two identical containers either in an ostensive-communicative (O) or in a nonostensive (NO) manner. In the ostensive condition, the human actor overtly expressed her communicative intent, whereas in the nonostensive condition, we removed the ostensive signal from the stimulus. Each trial consisted of introductory, addressing, and cueing phases ( Figures 1 A–1C ). All dogs participated in both O and NO trials that were different only in the addressing phase.

We obtained valid data for analysis from 13 dogs in the ostensive and 14 dogs in the nonostensive condition; however, only 11 of them provided valid data in each of these conditions (for the validity criteria see Data Analysis ). In the addressing phase, dogs spent similar amounts of time gazing toward the human actor in the two conditions (mean ± SEM: 1,088.8 ± 181.1 ms in O and 980.9 ± 267.8 ms in NO conditions, ns) and invested a comparable amount of time scanning the region containing the actor's face relative to the whole body: mean ± SEM = 0.46 ± 0.09 in the O condition and 0.55 ± 0.10 in the NO condition [paired t test t(10) = −0.88; p = 0.39] showing that in the addressing phase, the human actor evoked the same level of visual attention in both conditions.

1 Senju A.

Csibra G. Gaze following in human infants depends on communicative signals. 1 Senju A.

Csibra G. Gaze following in human infants depends on communicative signals. Figure 2 Difference Scores Calculated in O and NO Conditions for Different Measures of Gaze Following Show full caption ∗p < 0.05; error bars represent SEM. Next we analyzed whether dogs looked longer at the gaze-congruent area ( Figure 1 D) as compared to the gaze-incongruent area (cumulative accuracy). In accordance with infant eye-tracking studies (e.g., []), difference scores were calculated for this variable. We found that subjects looked longer to the gaze-congruent area than to the gaze-incongruent area after having seen ostensive addressing (one sample t test, t(12) = 2.382; p = 0.034). However, this was not the case for the nonostensive condition in which the difference score did not differ from zero [one-sample t test, t(13) = −0.756; p = 0.46], indicating no tendency to follow the human's gaze in the absence of communicative addressing ( Figure 2 ). This differential sensitivity to human referential gestures is strikingly similar to that found in a study of 6.5-month-old human infants []. A similar analysis on dogs' first look did not reveal any significant bias toward the gaze-congruent area in O or in the NO conditions [one-sample t test, t(12) = 1.167; p = 0.266; t(13) = −0.105; p = 0.91, Figure 2 ].

A within subject analysis of the difference scores for cumulative looking time in the two experimental conditions was run on the 11 subjects that gave valid data in both conditions. This analysis shows that dogs were more likely to follow the model's gaze in a gaze-congruent manner in the O than in the NO condition [t(10) = 2.49; p = 0.03; the effect was independent of presentation order; see Supplemental Results available online]. However, no difference was found between conditions for the first look [t(10) = −1.21; p = 0.25].

Figure 3 The Temporal Dynamic of the Eye Movements during the Cueing Phase in O and NO Conditions Show full caption The gaze data recorded from the lower half of the screen capture the main trends of eye movements (with gaze coordinates projected to x axis; resolution X = 1,280 pixels) as the mean gaze points move away from the midline of the display toward the GC or GIC region. After the actor's head movement, there is a peak that differs significantly from the central axis of the display only during the ostensive condition (∗p < 0.05; error bars represent SEM, 1° visual angle is approximately 40 pixels; y axis represents time). We also explored the spatiotemporal pattern of eye movements during cueing phase, investigating how the gaze points move away from the midline of the display and approach the target objects. Gaze points were averaged into 1 s bins and were projected to the x axis of the display ( Figure 3 ). The averaged eye movements showed a greater proximity to the target object only in the ostensive condition.

1 Senju A.

Csibra G. Gaze following in human infants depends on communicative signals. Thus, we may conclude that dogs' context-dependent responsiveness to human head turning mirrors the specific effect of human ostensive communication on dogs' cognitive processing. Although the stimuli in the two conditions were equally successful in orienting dogs' attention toward the actor's head in the addressing phase, only the ostensive cues led to gaze following. However, in order to elicit a comparable saliency of the addressing phases in the two conditions in the NO condition, we displayed a moving attention-getter on the model's forehead ( Figure 1 C) similar to the infant study []. Importantly, this raises the possibility that not the absence of ostensive cues but the artificial nature of this stimulus has contributed to the reduced gaze following in the NO condition.

To exclude this, we measured the gaze-following behavior of 13 additional experimentally naive dogs in a baseline control condition (BC) in which (1) the human actor turned her head without providing any ostensive cues (eye contact and addressing), (2) the salient attention-getter was removed from the addressing phase, and (3) the verbal addressing was replaced with neutral beep sound of similar duration and intensity in order to keep the auditory marking of this sequence comparable, while attracting the dogs' attention to the screen.

The data showed that gazing toward the region containing the actor's face relative to the whole body in the addressing phase was comparable to that found in O and NO conditions (mean ± SEM, 0.60 ± 0.07). However, dogs looked longer toward the body of the protagonist in both O and NO conditions than in BC [400.2 ± 106.9 ms; two-sample t tests: O versus BC t(21) = −3.44, p = 0.002; NO versus BC t(21) = −2.187, p = 0.04]. Thus, the combination of visual and audio components of the stimuli available in the addressing phase of O and NO conditions (direct gaze and infant-directed speech or visual grabber and adult-directed speech) attracted more attention toward the human actor. Importantly, however, the accuracy indexes calculated for the cueing phase did not capture gaze following in BC [mean ± SEM of cumulative accuracy: −0.06 ± 0.14; one-sample t test, t(12) = −0.433; p = 0.67; first look: 0.11 ± 0.16; one-sample t test, t(12) = 0.695; p = 0.5]. Furthermore, dogs followed the actor's gaze significantly less in the BC compared to the O condition [cumulative accuracy, two-sample t test, t(24) = −2.107, p = 0.045]. These data suggest that the lack of gaze following, when there are no ostensive signals, cannot be accounted for by the confounding effect of “artificial” salient attention getter used in the NO condition, also providing further support for the significant role of ostensive signals in dogs' gaze response.