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Brain Directed Connectivity Analysis Shows Evidence of Auditory Corollary Discharge

Poster E35 in Poster Session E, Saturday, October 8, 3:15 - 5:00 pm EDT, Millennium Hall
Also presenting in Poster Slam E, Saturday, October 8, 3:00 - 3:15 pm EDT, Regency Ballroom

Amirhossein Khalilian-Gourtani¹, Ran Wang¹, Xupeng Chen¹, Leyao Yu¹, Werner Doyle¹, Orrin Devinsky¹, Yao Wang¹, Adeen Flinker¹; ¹New York University

Introduction: A direct consequence of any motor action is the activation of the relevant sensory system. It is critical for the brain to dissociate self-generated action from external sensation. A hallmark neural circuit addresses this issue by a blueprint of motor signals informing the sensory cortex of the impending action; known as corollary discharge (CD). While there is ample evidence of CD signals across the animal kingdom and sensory modalities, the source and dynamics of CD in the human auditory system are not known. Methods: We leveraged the excellent spatiotemporal resolution of electrocorticography (ECoG) and acquired re-cordings from 8 neurosurgical patients while they performed an auditory repetition task (subjects were instructed to listen and then repeat single words). We used the high-gamma broadband (70-150 Hz) signal which is a common marker for underlying neural activity. In order to study the information flow between brain regions, we developed a directed connectivity analysis framework based on autoregressive Granger causality measures and applied unsupervised clustering techniques. Our approach elucidates dominant information flow (source and target) as well as prototypical temporal connectivity patterns (tested against permutation at p<0.05 for statistical significance) with their corresponding directed connections. Results: To understand the dynamics of information flow we applied our directed connectivity analysis framework to the neural recordings. Our results show three distinct phases during the auditory repetition task likely related to comprehension, pre-articulatory preparation, and speech production. Locked to word articulation we find a distinct component peaking at -100 msec relative to articulation onset with directed influence from speech motor cortex onto auditory cortex (STG). Unlike high-gamma analysis alone, which revealed pre-articulatory neural activity in multiple cortical regions and subsequent STG suppression, only the connectivity approach was able to extract the directed information flow which originated in ventral precentral gyrus targeting STG. The corollary discharge component replicated within patients and the degree of directed influence on auditory electrodes significantly predicted speech-induced suppression in STG (Pearson Correlation, R=0.504, p=5.3e-4). Conclusions: In humans, an auditory CD is hypothesized to increase sensitivity to our own speech and its impairment can lead to auditory hallucinations. Our results provide the first evidence for the source and timing of a corollary discharge signal in the human auditory system and has great implication for speech motor control as well as the study of psychotic symptoms in humans.

Topic Areas: Speech Motor Control, Language Production