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Does the head tilt observed in many domesticated dogs index lateralized language processing? To answer this question, the present study evaluated household dogs responding to four conditions in which owners provided an increasing number of communicative cues. These cues ranged from no communicative/affective cues to rich affective cues coupled with dog-directed speech. Dogs’ facial responses were first coded manually using the Dog Facial Action Coding System (DogFACS), followed by an in-depth investigation of head tilt behavior, in which AI-based automated analysis of head tilt and audio analysis of acoustic features extracted from communicative cues were implemented. In a sample of 103 dogs representing seven breed groups and mixed-breed dogs, we found significant differences in the number of head tilts occurring between conditions, with the most communicative (last) condition eliciting the most head tilts. There were also significant differences in the direction of the head tilts and between sex groups. Dogs were more likely to tilt their heads to the right, and neutered male dogs were more likely to tilt their heads than spayed female dogs. The right-tilt bias is consistent with left-hemisphere language processing in humans, with males processing language in a more lateralized manner, and females processing language more bilaterally—a pattern also observed in humans. Understanding the canine brain is important to both evolutionary research through a comparative lens, and in understanding our interspecies relationship.