The corollary discharge in humans is related to synchronous neural oscillations
Open accessAbstract
How do animals distinguish between sensations coming from external sources and those resulting from their own actions? A corollary discharge system has evolved that involves the transmission of a copy of motor commands to sensory cortex, where the expected sensation is generated. Through this mechanism, sensations are tagged as coming from self, and responsiveness to them is minimized. The present study investigated whether neural phase synchrony between motor command and auditory cortical areas is related to the suppression of the auditory cortical response. We recorded electrocorticograms from the human brain during a vocalizing/listening task. Neural phase synchrony between Broca's area and auditory cortex in the gamma band (35 to ∼50 Hz) in the 50-msec time window preceding speech onset was greater during vocalizing than during listening to a playback of the same spoken sounds. Because prespeech neural synchrony was correlated (r = −.83, p = .006), with the subsequent suppression of the auditory cortical response to the spoken sound, we hypothesize that phase synchrony in the gamma band between Broca's area and auditory cortex is the neural instantiation of the transmission of a copy of motor commands. We suggest that neural phase synchrony of gamma frequencies may contribute to transmission of corollary discharges in humans.
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L-IFG is invariably part of the corollary discharge network according to computational and neuroanatomical models of speech production.
“The lack of convergence in L-IFG is of interest as it is invariably a part of the corollary discharge network according to computational and neuroanatomical models of speech production (Chen et al., 2011; Tourville & Guenther, 2011).”
From Bridging phenomenology and neural mechanisms of inner speech: ALE meta-analysis on egocentricity and spontaneity in a dual-mechanistic framework (2023) · cites this paper as Chen et al., 2011
The Discussion describes the DIVA model’s speech-sound map as hypothesized to lie in the left posterior inferior frontal gyrus, with projections to auditory regions. The Introduction also describes a plausible route from Broca’s area to auditory cortex. These passages support L-IFG’s proposed role, but not the stronger claim that it is invariably part of the network across computational and neuroanatomical models; the indexed copy provides no page numbers. (LLM, conf=0.87)
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Cites
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“This can be interpreted as a gamma-band mediated neural instantiation of the transmission of a copy of motor commands (Chen et al., 2011).”
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“7 Corollary discharge mechanisms require a millisecond coordination between expected and unexpected neuronal events and preliminary evidence indicates that this process may be mediated by gamma-band activity during normal brain functioning [58].”
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“This study was recently replicated by the use of neural phase synchrony (Chen et al., 2011).”
MethodInsights into Cortical Oscillations Arising from Optogenetic Studies
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“We subsequently replicated and extended this finding in a similar group of patients (Chen, et al., 2011).”
ResultSelf-citationAttenuation of responses to self-generated sounds in auditory cortical neurons
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“…to such self-generated sounds are attenuated: smaller responses are evoked by subjects’ own speech sounds (Curio et al., 2000; Ford et al., 2001; Chen et al., 2011) or by manually triggered sounds (Schafer and Marcus, 1973; Martikainen et al., 2005; Baess et al., 2011) than when the same…”
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“The neurophysiology of the corollary discharge during vocalization has been studied across the animal kingdom, from songbirds (Keller and Hahnloser, 2009), crickets (Poulet and Hedwig, 2006) and bats (Suga and Shimozawa, 1974) to non-human primates (Eliades and Wang, 2003, 2005, 2008) and humans (Chen et al., 2011; Cr…”
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“Gamma-band oscillations, which are related to the interplay between PV+ interneurons and pyramidal neurons, have been associated with corollary discharges related to selfgenerated speech (Chen et al. 2010).”
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“For example, neural activity in the auditory cortex is markedly attenuated in response to hearing oneself speak, relative to hearing the same sounds played back in a passive listening condition (6-9).”
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“The efference copy and corollary discharge mechanisms have been studied during vocalization using invasive techniques across the animal kingdom, from crickets and bats to marmoset monkeys and humans [18,23–29].”
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“Modulation of auditory cortex during vocalization has been studied across species, including songbirds (6), non-human primates (7), and humans (8-20), and is posited to be mediated by predictive coding.”
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“Recording directly from the human brain, we reported that neural phase synchrony in the gamma band between Broca’s area and auditory cortex in the 50ms time window preceding speech onset was greater during speaking than listening and was correlated with suppression of N1 recorded from auditory cortex (Chen et al., 201…”
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“For example, the N100 (N1) component of the auditory event-related potential (ERP) elicited by sounds, and its counterpart in magnetoencephalographic recordings (M100), are reduced in amplitude in response to vocalizations as they are produced relative to when they are played back (Curio et al., 2000; Ford et al., 200…”
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“By 200 ms, there was a consistent pattern of co-variation between increased P200 amplitude, increased activation of bilateral STG/MTG, increased activation of frontal and parietal regions, and reduced activation ofMPFC, PCC, and visual cortex.”
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“Consequently, brain activity directed to incoming sensation is suppressed (Chen et al, 2011).”
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“A later study using electrocorticography also indicated that prespeech gamma synchrony between Broca’s area and auditory cortex was associated with the size of subsequent event related potentials (Chen et al., 2011).”
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“2013), intracranial recordings (Crone et al. 2006; Chen et al. 2011), and MNE source reconstruction (Gow et al.”
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“, 2012), or on the thalamus (Ostendorf, Liebermann, & Ploner, 2010; Bellebaum, Hoffmann, Koch, Schwarz, & Daum, 2006; Bellebaum, Daum, Koch, Schwarz, & Hoffmann, 2005), direct neural evidence of anticipatory sensory activity as a result of such motor-induced predictions is sparse (Chen et al., 2011; Kühn et al., 2010)…”
BackgroundInfluentialChanges in motor preparation affect the sensory consequences of voice production in voice hearers.
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“This finding was surprising, given that the temporal dynamics and tight linkage between N1 suppression and pre-speech activity are well-documented in TDC (Houde and Jordan, 2002; Eliades and Wang, 2003, 2005; Ford and Mathalon, 2005; Ford et al. , 2010; Chen et al. , 2011; Price et al. , 2011).”
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“The lack of convergence in L-IFG is of interest as it is invariably a part of the corollary discharge network according to computational and neuroanatomical models of speech production (Chen et al., 2011; Tourville and Guenther, 2011).”
BackgroundConsider the pons: Bridging the gap on sensory prediction abnormalities in schizophrenia
Abram, S. V., Hua, J., & Ford, J. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.08.008 · Cited by 23 · see citing works
Self-citationCorollary Discharge Mechanisms during Vocal Production in Marmoset Monkeys
Eliades, S., & Wang, X. (2019) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.06.008 · Cited by 23 · see citing works
Beño‐Ruiz‐de‐la‐Sierra, R. M., Arjona, A., Hernández-García, M., Fernández‐Linsenbarth, I., Díez, Á., Fondevila, S., Castaño, C., Muñoz, F., Sanz-Fuentenebro, J., Roig-Herrero, A., et al. (2023) · Schizophrenia Bulletin · doi:10.1093/schbul/sbad157 · Cited by 23 · see citing works
Ford, J. M., & Hoffman, R. E. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4121-2_19 · Cited by 17 · see citing works
Self-citationAuditory prediction during speaking and listening
Sato, M., & Shiller, D. (2018) · Brain and Language · doi:10.1016/j.bandl.2018.01.008 · Cited by 19 · see citing works
“Although evidence linking auditory neural suppression to motor cortex activity during speaking is sparse (Chang et al., 2013; Chen et al., 2011; Wang et al., 2014), the amplitude reduction of auditory evoked responses is most often interpreted as a consequence of efference copy and corollary discharge acting on the ne…”
Roach, B., Ford, J., Biagianti, B., Hamilton, H. K., Ramsay, I., Fisher, M., Loewy, R., Vinogradov, S., & Mathalon, D. (2018) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2018.12.015 · Cited by 18 · see citing works
“, 2002) and critical in N1 suppression (Chen et al., 2011; Wang et al., 2014).”
BackgroundSelf-citationSchizophrenia and Corollary Discharge: A Neuroscientific Overview and Translational Implications
Parlikar, R. U., Bose, A., & Venkatasubramanian, G. (2019) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2019.17.2.170 · Cited by 18 · see citing works
Roach, B., Ford, J., Loewy, R., Stuart, B. K., & Mathalon, D. (2020) · Schizophrenia bulletin · doi:10.1093/schbul/sbaa110 · Cited by 15 · see citing works
Self-citationAbram, S. V., Hua, J. P. Y., Nicholas, S., Roach, B., Keedy, S., Sweeney, J. A., Mathalon, D., & Ford, J. M. (2024) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2024.01.010 · Cited by 12 · see citing works
Self-citationRummell, B., Bikas, S., Babl, S. S., Gogos, J. A., & Sigurdsson, T. (2023) · Nature Communications · doi:10.1038/s41467-023-42964-2 · Cited by 10 · see citing works
Moon, J., Orlandi, S., & Chau, T. T. (2022) · Brain Research · doi:10.1016/j.brainres.2022.147778 · Cited by 15 · see citing works
Speech-induced suppression during natural dialogues
Gonzalez, J. E., Nieto, N., Brusco, P., Gravano, A., & Kamienkowski, J. (2024) · Communications Biology · doi:10.1038/s42003-024-05945-9 · Cited by 10 · see citing works
“TheSISeffectisproposedtobegeneratedbytheefferencecopyof theexpectedoutputofthespeaker ’ s own voice, sent to the primary auditory cortex (Helsch ’ s area) to cancel such signal from the perceived stimulus 61 .”
BackgroundKobayashi, K., Shiba, Y., Honda, S., Nakajima, S., Fujii, S., Mimura, M., & Noda, Y. (2024) · Brain Science · doi:10.3390/brainsci14020131 · Cited by 10 · see citing works
“Interestingly, these three functionally coupled regions are structurally connected via the auditory white-matter pathway, which was revealed by Oestreich, et al. [79] using diffusion magnetic resonance imaging (dMRI) and EEG.”
BackgroundLópez-Silva, P., Cavieres, Á., & Humpston, C. S. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.826654 · Cited by 10 · see citing works
“Normally, the frontal lobe sends an inhibitory signal to the auditory cortex (corollary discharge), minimizing the perception of the sensory reafference of the individual’s own speech (81).”
BackgroundEchoes on the motor network: how internal motor control structures afford sensory experience
Burgess, J. D., Lum, J. A. G., Hohwy, J., & Enticott, P. G. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1484-1 · Cited by 11 · see citing works
Skipper, J. I., & Hasson, U. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/139550 · Cited by 8 · see citing works
“…human vocal learning and speech production (Brown, Ingham, Ingham, Laird, & Fox, 2005; Chang, Niziolek, Knight, Nagarajan, & Houde, 2013; C.-M. A. Chen et al., 2011; Guenther, Ghosh, & Tourville, 2006; Kingyon et al., 2015; Niziolek, Nagarajan, & Houde, 2013; Rummell, Klee, & Sigurdsson, 2016;…”
Beño-Ruiz-de-la-Sierra, R., Arjona-Valladares, A., Estevez, S. F., Fernández-Linsenbarth, I., Díez, Á., & Molina, V. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.16125 · Cited by 8 · see citing works
Hallucination Proneness Alters Sensory Feedback Processing in Self-voice Production
Duggirala, S., Schwartze, M., Goller, L., Linden, D., Pinheiro, A., & Kotz, S. (2023) · bioRxiv · doi:10.1093/schbul/sbae095 · Cited by 8 · see citing works
Motor and visual influences on auditory neural processing during speaking and listening.
Sato, M. (2022) · Cortex; a journal devoted to the study of the nervous system and behavior · doi:10.1016/j.cortex.2022.03.013 · Cited by 7 · see citing works
Analgesia induced by self-initiated electrotactile sensation is mediated by top-down modulations.
Zhao, K., Tang, Z., Wang, H., Guo, Y.-F., Peng, W., & Hu, L. (2017) · Psychophysiology · doi:10.1111/psyp.12839 · Cited by 7
“…the anticipatory modulation of sensory neural processing from motor actions, and self-initiated action-induced attenuation of sensory perception was mainly caused by top-down modulations mediated by motorinduced sensory anticipation (Chen et al., 2011; Kuhn, Seurinck, Fias, & Waszak, 2010).”
BackgroundSingle-Trial Classification of Disfluent Brain States in Adults Who Stutter
Myers, J. C., Irani, F., Golob, E. J., Mock, J. R., & Robbins, K. A. (2018) · Conference proceedings/Conference proceedings - IEEE International Conference on Systems, Man, and Cybernetics · doi:10.1109/smc.2018.00019 · Cited by 4 · see citing works
“Therefore, coherence between ICs could capture synchrony and functional connectivity between two brain regions [13].”
So, R. P., Kegeles, L., Mao, X., Shungu, D., Stanford, A. D., & Chen, C.-M. A. (2018) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2017.1420142 · Cited by 6 · see citing works
“dysfunctions in Broca’s area and auditory cortical regions (Chen et al., 2011; Ford, Gray, Faustman, Heinks, & Mathalon, 2005).”
BackgroundMethodSelf-citationGriffiths, O., Jack, B. N., Pearson, D., Elijah, R., Mifsud, N. G., Han, N., Libesman, S., Barreiros, A. R., Turnbull, L., Balzan, R., et al. (2022) · NeuroImage: Clinical · doi:10.1016/j.nicl.2022.103290 · Cited by 5 · see citing works
Vocalizing and singing reveal complex patterns of corollary discharge function in schizophrenia
Ford, J. M., Roach, B. J., & Mathalon, D. H. (2021) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2021.02.013 · Cited by 5 · see citing works
Self-citationWhitford, T. J., Spencer, K., Godwin, M., Hirano, Y., Chung, L. K.-H., Vodovozov, W., Griffiths, O., Harris, A. W. F., Pelley, M. E. L., & Jack, B. N. (2025) · eNeuro · doi:10.1523/eneuro.0297-24.2025 · Cited by 8 · see citing works
“…et al., 2016); thirdly, studies investigating gamma-band coherence between the frontal and temporal lobes have found coherence to be higher during overt speech production compared with listening (Chen et al., 2011) and to predicted versus unpredicted auditory feedback (Ford et al., 2005).”
Beño‐Ruiz‐de‐la‐Sierra, R. M., Arjona, A., Hernández-García, M., Fernández‐Linsenbarth, I., Díez, Á., Roig-Herrero, A., Osorio-Iriarte, E., & Molina, V. (2024) · Clinical Neurophysiology · doi:10.1016/j.clinph.2024.07.014 · Cited by 6 · see citing works
Sharma, G., Chitturi, V., Sharma, V., Kathrotia, R., Barde, P., Parmar, N., Sharma, M., & Singh, R. (2024) · Scientific Reports · doi:10.1038/s41598-024-67279-0 · Cited by 4
Alhazmi, F. (2025) · Brain Science · doi:10.3390/brainsci15090914 · Cited by 3 · see citing works
“Some studies suggest that impaired brain processes, such as an inability to suppress self-generated sounds, may play a role, potentially paving the way for new treatment strategies [9–11].”
Kusztrits, I., Marquardt, L., Hugdahl, K., & Hirnstein, M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0257010 · Cited by 5 · see citing works
“In addition, Chen, Mathalon [46] suggested that Broca’s area is also involved in a process called auditory corollary discharge.”
BackgroundSolbakk, A., Lubell, J. I., Leske, S., Funderud, I., Llorens, A., Blenkmann, A., Foldal, M., Meling, T., Knight, R., & Endestad, T. (2021) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01733 · Cited by 2 · see citing works
“It suggests that, if an action is self-produced, an efference copy of the motor command is generated to predict the sensory consequences of an action, thereby reducing the processing activity related to the expected sensory outcome (Chen et al., 2011).”
BackgroundVoces que No lo Son: Los Problemas del Concepto Pseudoalucinación
López-Silva, P., & Cavieres-Fernández, A. (2020) · Revista chilena de neuro-psiquiatría · doi:10.4067/s0717-92272020000100029 · Cited by 2 · see citing works
Antonicelli, G., Morin, B. T., Bogley, R., Newbury, R., Ezzes, Z., Ramkrishnan, S., Miller, Z., Mandelli, M. L., Tee, B. L., García, A. M., et al. (2026) · Cortex · doi:10.1016/j.cortex.2026.10.006
Samantaray, S., Goyal, N., Kesavan, M., Venkatasubramanian, G., Shreekantiah, U., Bose, A., Sreeraj, V., Das, M., Raj, J., & Kumar, S. (2025) · Schizophrenia Research · doi:10.1016/j.schres.2025.07.003 · Cited by 1 · see citing works
Moon, J., & Chau, T. (2023) · Speech Communication · doi:10.2139/ssrn.4184639 · Cited by 1 · see citing works
A comparison of oscillatory characteristics in covert speech and speech perceptionPreprint
Moon, J., Orlandi, S., & Chau, T. (2020) · arXiv (Cornell University) · doi:10.48550/arxiv.2009.02816 · Cited by 1 · see citing works
“It is possible that the γ-band activity during CS corresponded to a corollary discharge, as enhanced fronto-temporal γ synchrony has been observed during speech production tasks relative to perception conditions (Chen et al., 2011; Ford and Mathalon, 2005).”
BackgroundFord, J. M., Roach, B., Loewy, R., Stuart, B. K., & Mathalon, D. (2019) · bioRxiv · doi:10.1101/563460 · Cited by 1
“We further suggest that during talking, a corollary discharge of the motor command is sent to auditory cortex (Chen et al., 2011, Wang et al., 2014).”
BackgroundSelf-citationHoude, J. F., & Nagarajan, S. (2015) · doi:10.1002/9781118584156.ch13 · Cited by 1 · see citing works
Beño-Ruiz-de-la-Sierra, R., Arjona-Valladares, A., Osorio-Iriarte, E., Sobrino-Conde, L., Rodríguez, V., Núñez, P., Poza, J., Roig-Herrero, A., Díez, Á., & Molina, V. (2026) · Schizophrenia Research · doi:10.1016/j.schres.2026.09.038
Makibuchi, T., Anazawa, S., Hagino, Y., Fujimoto, T., Ochi, G., Sato, D., & Yamashiro, K. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70654
“…and Kakigi 2006; Kida, Wasaka, Nakata, Akatsuka, and Kakigi 2006b), auditory (Curio et al. 2000; Ford et al. 2001; Heinks-Maldonado et al. 2005; Chen et al. 2011), and visual systems (Hughes and Waszak 2011), although the temporal and functional characteristics of this modulation appear to…”
Jia, Y., Kudo, K., Jariwala, N., Tarapore, P. E., Nagarajan, S. S., & Subramaniam, K. (2024) · medRxiv · doi:10.1101/2024.02.13.24302764
“…are consistent with prior studies that have shown increased neural activity in mPFC, extending to regions such as CG and PCL, in lower frequency alpha and theta bands, which is thought to reflect feedforward predictive coding models that model the expected sensory outcome of self-generated…”
Online decoding of covert speech based on the passive perception of speechPreprint
Moon, J., & Chau, T. (2022) · bioRxiv · doi:10.1101/2022.11.13.516334
“This finding is consistent with reports of γ activity being implicated in corollary 612 discharge (34,75), a mechanism thought to deliver temporally precise and content-specific 613 sensory predictions of speech (76).”
ResultBASES COGNITIVAS DA EXPECTATIVA TEMPORAL
Cravo, A. M. (2011) · doi:10.11606/t.42.2011.tde-22072011-083628
Dynamics and energy dissipation analysis of a memristive neural circuit lossing capacitors
Guo, Q., & Xu, Y. (2026) · Acta Physica Sinica · doi:10.7498/aps.75.20251114
Analysis of dynamics and energy consumption in capacitor-free memristive neural circuit
Guo, Q., & Xu, Y. (2026) · Acta Physica Sinica · doi:10.7498/aps.74.20251114
- Authors
- Chen, C.-M. A., Mathalon, D. H., Roach, B. J., Cavus, I., Spencer, D. D., & Ford, J. M.
- Affiliations
- Yale University (US)
- University of California, San Francisco (US)
- 2Yale University
- Venue
- Journal of Cognitive Neuroscience
- Publisher
- MIT Press - Journals
- Published
- 2011-10-01
- Volume
- 23
- Issue
- 10
- Pages
- 2892-2904
- ISSN
- 0898-929X (ISSN-L)
- 1530-8898
- PMC
- PMC4155919
- OpenAlex
- W2165282941
- Cited by
- 86
- References
- 88
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 10 · 2023: 5 · 2022: 7 · 2021: 3 · 2020: 5 · 2019: 6 · 2018: 7 · 2017: 4 · 2016: 7 · 2015: 4 · 2014: 3 · 2013: 4 · 2012: 6
- FWCI
- 3.10
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Cognitive Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5r01mh058262-17)
- National Institute of Mental Health (R01MH-058262)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- corollary discharge, gamma oscillations, Broca's area, auditory cortex, speech production, electrocorticography
- MeSH terms
- Adult, Analysis of Variance, Auditory Cortex, Brain Mapping, Electroencephalography, Epilepsy, Evoked Potentials, Auditory, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Neural Pathways, Reaction Time, Electroencephalography Phase Synchronization
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