Lip-reading on the left, eye-gaze on the right? Causal evidence for functional lateralisation in face-selective posterior superior temporal sulcus.
DOI: Pending DOI
Synopsis
Posterior superior temporal sulcus (pSTS) processes facial cues that are critical for social perception, including information from the eyes and mouth. To investigate whether bilateral face-selective pSTS shows hemispheric specialisation for different facial cues, we combined TMS and resting-state fMRI across three experiments. TMS over the left pSTS selectively impaired lip discrimination and lip-reading, whereas TMS over the right pSTS selectively impaired eye-gaze discrimination, demonstrating a double dissociation. Resting-state connectivity analyses showed stronger connectivity between the left pSTS and language-related regions, and between the right pSTS and face- and attention-related regions. These findings suggest that different facial cues may be causally processed by different hemispheres within face-selective pSTS, supporting parallel processing of distinct socially relevant facial cues.
Background
Human social interaction relies on the ability to perceive and interpret social cues [1]. Converging evidence from neuroimaging, neuropsychology, and brain stimulation implicates the pSTS as a key region supporting these processes by responding to diverse social signals such as facial emotion, eye-gaze direction, and speech-related mouth movements [2-6]. While this body of work establishes a causal role for the pSTS in social perception, it remains unclear whether these functions are organised in a hemispherically specialised manner and whether any such lateralisation depends on the type of social cues being processed.
Evidence for hemispheric asymmetry is mixed. Studies of facial expression recognition and eye-gaze perception often report a right pSTS bias, supported by functional imaging, lesion evidence, and TMS [7-14]. In contrast, processing of visual speech and audiovisual integration appears more bilateral, with some findings suggesting a left hemisphere contribution linked to language networks [15-19]. However, prior studies often focus on one hemisphere in isolation, limiting direct comparisons of left and right pSTS function.
Critically, different facial features convey distinct forms of social information: eye-gaze is linked to visuospatial attention and social orienting, whereas mouth movements are key to speech perception and audiovisual integration [1,20]. Whether these distinct facial cues are supported by causally dissociable left and right pSTS mechanisms remains unknown. Our previous TMS studies [21,22] demonstrated causal roles for both left and right pSTS in facial expression recognition but did not test whether hemispheric contributions differ according to the specific facial cue being processed. The present study addresses this gap by directly comparing left and right pSTS contributions across two different facial cues.
Methods
The study combined TMS and resting-state fMRI to investigate hemispheric specialisation for processing eye- and mouth-derived social cues within the bilateral face-selective pSTS. In Experiment 1, participants (N=18) performed lip-position and eye-gaze discrimination tasks in static facial expressions while TMS was delivered over the left and right pSTS. The behavioural paradigm and stimuli were adapted from our previous TMS studies [21,22] of facial expression processing to allow direct comparison with earlier findings. In Experiment 2, participants (N=16) completed a lip-reading task using dynamic, non-emotional video clips of a speaker while TMS was delivered over the left and right pSTS to assess whether hemispheric effects generalised to audiovisual speech processing. In Experiment 3, participants (N=256) underwent resting-state fMRI to examine large-scale functional connectivity profiles of the left and right face-selective TMS targets in pSTS and determine whether the causal dissociations observed during TMS corresponded to distinct connectivity patterns. Together, the experiments tested whether hemispheric specialisation within pSTS differs according to speech-related versus visuospatial social cues.
Results
In Experiment 1, results revealed a double dissociation in which disruption of the left pSTS impaired the lip-position discrimination task (see Experiment 1A), whereas disruption of the right pSTS impaired the eye-gaze discrimination task (see Experiment 1B). In Experiment 2, TMS impaired a lip-reading task when TMS was delivered over the left pSTS only (see Experiment 2). In Experiment 3, results demonstrated that the left pSTS exhibited greater connectivity to language-related brain areas in the left hemisphere. In contrast, the right pSTS exhibited greater connectivity to bilateral visual face and attention networks.
Discussion
Our findings demonstrate differential functional contributions of bilateral face-selective regions within the pSTS, with the left pSTS preferentially involved in lip and speech-related processing and the right pSTS preferentially involved in eye-gaze processing. These dissociations were supported by distinct large-scale functional connectivity profiles, suggesting that hemispheric specialisation within pSTS reflects broader differences between language and audiovisual speech networks in the left hemisphere and social attention networks in the right hemisphere. Such functional segregation may support parallel processing of socially relevant facial information during real-world interactions. These findings refine current neurological models of face perception by demonstrating functional segregation within bilateral pSTS and its integration with larger-scale language and social-attention networks. The findings may inform future investigations of neurodevelopmental and neurological conditions characterised by atypical social communication, including autism and acquired social perceptual impairments. Future work should examine how hemispheric specialisation within pSTS develops across the lifespan and how these networks are altered in clinical populations.
Disclosures
No conflicts of interest. This study was supported by a Biotechnology and Biological Sciences Research Council (BBSRC) New Investigator Grant [BB/BB/P006981 to DP] and a Leverhulme Trust Project Grant [RPG-2024-389 to DP] and has been accepted for publication by Cerebral Cortex (DOI: 10.1093/cercor/bhag088).
References
1. Frith CD, Frith U. 2012. Mechanisms of social cognition. Annu Rev Psychol. 63:287–313.
2. Allison T, Puce A, McCarthy G. 2000. Social perception from visual cues: role of the STS region. Trends Cogn Sci. 4(7):267–278.
3. Hein G, Knight RT. 2008. Superior temporal sulcus-it's my area: or is it? J Cogn Neurosci. 20(12):2125–2136.
4. Puce A, Allison T, Bentin S, Gore JC, McCarthy G. 1998. Temporal cortex activation in humans viewing eye and mouth movements. J Neurosci. 18(6):2188–2199.
5. Deen B, Koldewyn K, Kanwisher N, Saxe R. 2015. Functional organization of social perception and cognition in the superior temporal sulcus. Cereb Cortex. 25(11):4596–4609.
6. Schobert AK, Corradi-Dell'Acqua C, Fruhholz S, van der Zwaag W, Vuilleumier P. 2018. Functional organization of face processing in the human superior temporal sulcus: a 7T high-resolution fMRI study. Soc Cogn Affect Neurosci. 13(1):102–113.
7. Pitcher D, Walsh V, Yovel G, Duchaine B. 2007. TMS evidence for the involvement of the right occipital face area in early face processing. Curr Biol. 17(18):1568–1573.
8. Pitcher D, Dilks DD, Saxe RR, Triantafyllou C, Kanwisher N. 2011. Differential selectivity for dynamic versus static information in face-selective cortical regions. Neuroimage. 56(4):2356–2363.
9. Pitcher D, Pilkington A, Rauth L, Baker C, Kravitz DJ, Ungerleider L. 2020. The human posterior superior temporal sulcus samples visual space differently from other face-selective regions. Cereb Cortex. 30(2):778–785.
10. Winston JS, Henson RN, Fine-Goulden MR, Dolan RJ. 2004. fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J Neurophysiol. 92(3):1830–1839.
11. Calder AJ, Beaver JD, Winston JS, Dolan RJ, Jenkins R, Eger E, Henson RNA. 2007. Separate coding of different gaze directions in the superior temporal sulcus and inferior parietal lobule. Curr Biol. 17(1):20–25.
12. Akiyama T, Kato M, Muramatsu T, Saito F, Nakachi R, Kashima K. 2006. A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion. Neuropsychologia. 44(2):161–170.
13. Pourtois G, Sander D, Andres M, Grandjean D, Reveret L, Olivier E, Vuilleumier P. 2004. Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals. Eur J Neurosci. 20(12):3507–3515.
14. Engell AD, Haxby JV. 2007. Facial expression and gaze-direction in human superior temporal sulcus. Neuropsychologia. 45(14):3234–3241.
15. McGurk H, MacDonald J. 1976. Hearing lips and seeing voices. Nature. 264(5588):746–748.
16. Walker S, Bruce V, O'Malley C. 1995. Facial identity and facial speech processing: familiar faces and voices in the McGurk effect. Percept Psychophys. 57(8):1124–1133.
17. Alsius A, Navarra J, Campbell R, Soto-Faraco S. 2005. Audiovisual integration of speech falters under high attention demands. Curr Biol. 15(9):839–843.
18. Lee H, Noppeney U. 2011. Physical and perceptual factors shape the neural mechanisms that integrate audiovisual signals in speech comprehension. J Neurosci. 31(31):11338–11350.
19. Beauchamp MS, Nath AR, Pasalar S. 2010. fMRI-guided transcranial magnetic stimulation reveals that the superior temporal sulcus is a cortical locus of the McGurk effect. J Neurosci. 30(7):2414–2417.
20. Haxby JV, Hoffman EA, Gobbini MI. 2000. The distributed human neural system for face perception. Trends Cogn Sci. 4(6):223–233.
21. Sliwinska MW, Pitcher D. 2018. TMS demonstrates that both right and left superior temporal sulci are important for facial expression recognition. Neuroimage. 183:394–400.
22. Sliwinska MW, Elson R, Pitcher D. 2020. Dual-site TMS demonstrates causal functional connectivity between the left and right posterior temporal sulci during facial expression recognition. Brain Stimul. 13(4):1008–1013.
