Masaaki Nishida1, Anna Korzeniewska2, Nathan E Crone3, Goichiro Toyoda4, Yasuo Nakai4, Noa Ofen5, Erik C Brown6, Eishi Asano7. 1. Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit Medical Center, Detroit, MI 48201, USA; Department of Anesthesiology, Hanyu General Hospital, Hanyu City, Saitama 348-8508, Japan. 2. Department of Neurology, Johns Hopkins University, Baltimore, MD 21287, USA. Electronic address: akorzen@jhmi.edu. 3. Department of Neurology, Johns Hopkins University, Baltimore, MD 21287, USA. 4. Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit Medical Center, Detroit, MI 48201, USA. 5. Institute of Gerontology, Wayne State University, Detroit, MI 48202, USA; Department of Psychology, Wayne State University, Detroit, MI 48202, USA. 6. Department of Neurosurgery, Oregon Health and Science University, Portland, OR, USA. 7. Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit Medical Center, Detroit, MI 48201, USA; Department of Neurology, Children's Hospital of Michigan, Wayne State University, Detroit Medical Center, Detroit, MI 48201, USA. Electronic address: easano@med.wayne.edu.
Abstract
OBJECTIVE: The articulatory loop is a fundamental component of language function, involved in the short-term buffer of auditory information followed by its vocal reproduction. We characterized the network dynamics of the human articulatory loop, using invasive recording and stimulation. METHODS: We measured high-gamma activity70-110 Hz recorded intracranially when patients with epilepsy either only listened to, or listened to and then reproduced two successive tones by humming. We also conducted network analyses, and analyzed behavioral responses to cortical stimulation. RESULTS: Presentation of the initial tone elicited high-gamma augmentation bilaterally in the superior-temporal gyrus (STG) within 40ms, and in the precentral and inferior-frontal gyri (PCG and IFG) within 160ms after sound onset. During presentation of the second tone, high-gamma augmentation was reduced in STG but enhanced in IFG. The task requiring tone reproduction further enhanced high-gamma augmentation in PCG during and after sound presentation. Event-related causality (ERC) analysis revealed dominant flows within STG immediately after sound onset, followed by reciprocal interactions involving PCG and IFG. Measurement of cortico-cortical evoked-potentials (CCEPs) confirmed connectivity between distant high-gamma sites in the articulatory loop. High-frequency stimulation of precentral high-gamma sites in either hemisphere induced speech arrest, inability to control vocalization, or forced vocalization. Vocalization of tones was accompanied by high-gamma augmentation over larger extents of PCG. CONCLUSIONS: Bilateral PCG rapidly and directly receives feed-forward signals from STG, and may promptly initiate motor planning including sub-vocal rehearsal for short-term buffering of auditory stimuli. Enhanced high-gamma augmentation in IFG during presentation of the second tone may reflect high-order processing of the tone sequence. SIGNIFICANCE: The articulatory loop employs sustained reciprocal propagation of neural activity across a network of cortical sites with strong neurophysiological connectivity.
OBJECTIVE: The articulatory loop is a fundamental component of language function, involved in the short-term buffer of auditory information followed by its vocal reproduction. We characterized the network dynamics of the human articulatory loop, using invasive recording and stimulation. METHODS: We measured high-gamma activity70-110 Hz recorded intracranially when patients with epilepsy either only listened to, or listened to and then reproduced two successive tones by humming. We also conducted network analyses, and analyzed behavioral responses to cortical stimulation. RESULTS: Presentation of the initial tone elicited high-gamma augmentation bilaterally in the superior-temporal gyrus (STG) within 40ms, and in the precentral and inferior-frontal gyri (PCG and IFG) within 160ms after sound onset. During presentation of the second tone, high-gamma augmentation was reduced in STG but enhanced in IFG. The task requiring tone reproduction further enhanced high-gamma augmentation in PCG during and after sound presentation. Event-related causality (ERC) analysis revealed dominant flows within STG immediately after sound onset, followed by reciprocal interactions involving PCG and IFG. Measurement of cortico-cortical evoked-potentials (CCEPs) confirmed connectivity between distant high-gamma sites in the articulatory loop. High-frequency stimulation of precentral high-gamma sites in either hemisphere induced speech arrest, inability to control vocalization, or forced vocalization. Vocalization of tones was accompanied by high-gamma augmentation over larger extents of PCG. CONCLUSIONS: Bilateral PCG rapidly and directly receives feed-forward signals from STG, and may promptly initiate motor planning including sub-vocal rehearsal for short-term buffering of auditory stimuli. Enhanced high-gamma augmentation in IFG during presentation of the second tone may reflect high-order processing of the tone sequence. SIGNIFICANCE: The articulatory loop employs sustained reciprocal propagation of neural activity across a network of cortical sites with strong neurophysiological connectivity.
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