Neural correlates of human action observation in hearing and deaf subjects

Abstract

Accumulating evidence has suggested the existence of a human action recognition system involving inferior frontal, parietal, and superior temporal regions that may participate in both the perception and execution of actions. However, little is known about the specificity of this system in response to different forms of human action. Here we present data from PET neuroimaging studies from passive viewing of three distinct action types, intransitive self-oriented actions (e.g., stretching, rubbing one's eyes, etc.), transitive object-oriented actions (e.g., opening a door, lifting a cup to the lips to drink), and the abstract, symbolic actions-signs used in American Sign Language. Our results show that these different classes of human actions engage a frontal/parietal/STS human action recognition system in a highly similar fashion. However, the results indicate that this neural consistency across motion classes is true primarily for hearing subjects. Data from deaf signers shows a non-uniform response to different classes of human actions. As expected, deaf signers engaged left-hemisphere perisylvian language areas during the perception of signed language signs. Surprisingly, these subjects did not engage the expected frontal/parietal/STS circuitry during passive viewing of nonlinguistic actions, but rather reliably activated middle-occipital temporal-ventral regions which are known to participate in the detection of human bodies, faces, and movements. Comparisons with data from hearing subjects establish statistically significant contributions of middle-occipital temporal-ventral during the processing of non-linguistic actions in deaf signers. These results suggest that during human motion processing, deaf individuals may engage specialized neural systems that allow for rapid, online differentiation of meaningful linguistic actions from non-linguistic human movements.

Neural systems supporting linguistic structure, linguistic experience, and symbolic communication in sign language and gesture

“…This network is consistent with previous studies of both sign language and gesture that used similar contrasts with a low-level baseline (10,(22)(23)(24)(25)(26)(27). Critically, however, compared with the backwardlayered conditions that controlled for stimulus features (such as biological motion and face perception) and for motor responses, a much more restricted set of brain areas was activated, with considerably less overlap across groups and conditions.…”

“…This includes the inferior frontal gyrus (IFG) (classically called Broca's area), superior temporal sulcus (STS) and adjacent superior and middle temporal gyri, and the inferior parietal lobe (IPL) (classically called Wernicke's area) including the angular (AG) and supramarginal gyri (SMG) (4,(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). Likewise, narrative and discourse-level aspects of signed language depend largely on right STS regions, as they do for spoken language (17,19).…”

Decoding Actions and Emotions in Deaf Children: Evidence From a Biological Motion Task

“…Different experiences with manual communication might then alter the nature of the neural systems that underlie action for deaf signers (Corina et al, 2007) and thus differences in any system representing actions may lead to problems in social perception including Theory of Mind. Whilst problems in understanding other people's emotions have often been attributed directly to deaf children's lack of opportunity to converse it is possible that this may in fact be more specific to children signing experience.…”

“…One recent strand of research has provided evidence that deaf children adopt alternative perceptual strategies to hearing children. For example, they rely more heavily on motion cues whilst gauging when to cross a busy road (Bosworth & Dobkins, 2002) and when comprehending critical linguistic information in the hand movements of British sign language (Corina et al, 2007). It is surprising, given both the importance of motion for emotion understanding, and findings suggesting atypical motion processing in deaf children, that motion processing in communication domains has not been widely studied in this population.…”

“…In order to capitalize on their proven strengths in motion processing (Bosworth & Dobkins, 2002;Corina et al, 2007), we adopted the methods used by Parron et al (2008) and used PLDs to test the assumption of a global emotion-processing deficit in deaf children. Point lights techniques have been used previously with deaf populations to assess how sign language influences action processing (Knapp, Cho & Corina, 2008).…”