Dynamics of Auditory–Vocal Interaction in Monkey Auditory Cortex
Abstract
Single neurons in the primate auditory cortex exhibit vocalization-related modulations (excitatory or inhibitory) during self-initiated vocal production. Previous studies have shown that these modulations of cortical activity are variable in individual neurons' responses to multiple instances of vocalization and diverse between different cortical neurons. The present study investigated dynamic patterns of vocalization-related modulations and demonstrated that much of the variability in cortical modulations was related to the acoustic structures of self-produced vocalization. We found that suppression of single unit activity during multi-phrased vocalizations was temporally specific in that it was maintained during each phrase, but was released between phrases. Furthermore, the degree of suppression or excitation was correlated to the mean energy and frequency of the produced vocalizations, accounting for much of the response variability between multiple instances of vocalization. Simultaneous recordings of pairs of neurons from a single electrode revealed that the modulations by self-produced vocalizations in nearby neurons were largely uncorrelated. Additionally, vocalization-induced suppression was found to be preferentially distributed to upper cortical layers. Finally, we showed that the summation of all auditory cortical activity during vocalization, including both single and multi-unit responses, was weakly excitatory, consistent with observations from studies of the human brain during speech.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the marmoset primary auditory cortex, many neurons are suppressed during self-vocalizations.
“A protective mechanism is observable in the marmoset primary auditory cortex, where many neurons are suppressed during self-vocalizations27,28.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [28]
In marmosets, suppression begins about 200 ms before vocalization and continues for its duration.
“Suppression begins ~200 ms before vocalization and continues for its duration.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [28]
Cites
Das Reafferenzprinzip: Wechselwirkungen zwischen Zentralnervensystem und Peripherie
von Holst, E., & Mittelstaedt, H. (1950) · Naturwissenschaften · doi:10.1007/bf00622503 · Cited by 2,655 · see citing works
(1960) · Medical Journal of Australia · doi:10.5694/j.1326-5377.1960.tb76238.x · Cited by 2,178 · see citing works
Neural basis of the spontaneous optokinetic response produced by visual inversion
Sperry, R. W. (1950) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0055479 · Cited by 1,789 · see citing works
Central cancellation of self-produced tickle sensation
Blakemore, S.-J., Wolpert, D. M., & Frith, C. D. (1998) · Nature Neuroscience · doi:10.1038/2870 · Cited by 1,467 · see citing works
A review of methods for spike sorting: the detection and classification of neural action potentials
Lewicki, M. S. (1998) · Network Computation in Neural Systems · doi:10.1088/0954-898x_9_4_001 · Cited by 1,372 · see citing works
The Organization of Language and the Brain
Geschwind, N. (1970) · Science · doi:10.1126/science.170.3961.940 · Cited by 1,141 · see citing works
Processing of Complex Sounds in the Macaque Nonprimary Auditory Cortex
Rauschecker, J. P., Tian, B., & HAUSER, M. D. (1995) · Science · doi:10.1126/science.7701330 · Cited by 929 · see citing works
Sensorimotor Adaptation in Speech Production
Houde, J. F., & Jordan, M. I. (1998) · Science · doi:10.1126/science.279.5354.1213 · Cited by 770 · see citing works
Representation of the cochlear partition on the superior temporal plane of the macaque monkey
Merzenich, M. M., & Brugge, J. F. (1973) · Brain Research · doi:10.1016/0006-8993(73)90731-2 · Cited by 765 · see citing works
Gray, C. M., Maldonado, P., Wilson, M., & McNaughton, B. L. (1995) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(95)00085-2 · Cited by 746 · see citing works
The Lombard Sign and the Role of Hearing in Speech
Lane, H., & Tranel, B. (1971) · Journal of Speech and Hearing Research · doi:10.1044/jshr.1404.677 · Cited by 744 · see citing works
Representation of cochlea within primary auditory cortex in the cat
Merzenich, M. M., Knight, P. L., & Roth, G. (1975) · Journal of Neurophysiology · doi:10.1152/jn.1975.38.2.231 · Cited by 638 · see citing works
A Pathway in Primate Brain for Internal Monitoring of Movements
Sommer, M. A., & Wurtz, R. H. (2002) · Science · doi:10.1126/science.1069590 · Cited by 565 · see citing works
Synaptic physiology of horizontal connections in the cat's visual cortex
Hirsch, J., & Gilbert, C. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-06-01800.1991 · Cited by 532 · see citing works
Hackett, T. A., Preuss, T. M., & Kaas, J. H. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1407 · Cited by 522 · see citing works
Brain regions involved in articulation
Wise, R., Greene, J., Büchel, C., & Scott, S. (1999) · The Lancet · doi:10.1016/s0140-6736(98)07491-1 · Cited by 517 · see citing works
Voice F0 responses to manipulations in pitch feedback
Burnett, T. A., Freedland, M. B., Larson, C. R., & Hain, T. C. (1998) · The Journal of the Acoustical Society of America · doi:10.1121/1.423073 · Cited by 508 · see citing works
Temporal and rate representations of time-varying signals in the auditory cortex of awake primates
Lu, T., Li, L., & Wang, X. (2001) · Nature Neuroscience · doi:10.1038/nn737 · Cited by 465 · see citing works
Self-citationModulation of the Auditory Cortex during Speech: An MEG Study
Houde, J. F., Nagarajan, S. S., Sekihara, K., & Merzenich, M. M. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/089892902760807140 · Cited by 458 · see citing works
A PET study of the neural systems of stuttering
Fox, P. T., Ingham, R. J., Ingham, J. C., Hirsch, T. B., Downs, J. H., Martin, C. C., Jerabek, P., Glass, T. G., & Lancaster, J. L. (1996) · Nature · doi:10.1038/382158a0 · Cited by 452 · see citing works
Acoustic communication in noise: regulation of call characteristics in a New World monkey
Brumm, H., Voss, K., Köllmer, I., & Todt, D. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00768 · Cited by 361 · see citing works
An auditory domain in primate prefrontal cortex
Romanski, L. M., & Goldman‐Rakic, P. S. (2001) · Nature Neuroscience · doi:10.1038/nn781 · Cited by 358 · see citing works
Effects of Delayed Speech Feedback
Lee, B. S. (1950) · The Journal of the Acoustical Society of America · doi:10.1121/1.1906696 · Cited by 354 · see citing works
GATING OF SOMATOSENSORY EVOKED POTENTIALS DURING DIFFERENT KINDS OF MOVEMENT IN MAN
Rushton, D. N., ROGHWELL, J. C., & Craggs, M. D. (1981) · Brain · doi:10.1093/brain/104.3.465 · Cited by 345 · see citing works
Prefrontal connections of the parabelt auditory cortex in macaque monkeys
Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01182-2 · Cited by 343 · see citing works
Neuronal activity in the human lateral temporal lobe
Creutzfeldt, O. D., Ojemann, G. A., & Lettich, E. (1989) · Experimental Brain Research · doi:10.1007/bf00249600 · Cited by 335 · see citing works
Sensory-Motor Interaction in the Primate Auditory Cortex During Self-Initiated Vocalizations
Eliades, S. J., & Wang, X. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00627.2002 · Cited by 315 · see citing works
Self-citationDecrystallization of adult birdsong by perturbation of auditory feedback
Leonardo, A. M., & Konishi, M. (1999) · Nature · doi:10.1038/20933 · Cited by 314 · see citing works
Electrocorticographic gamma activity during word production in spoken and sign language
Crone, N. E., Hao, L., Hart, J., Boatman, D. F., Lesser, R. P., Irizarry, R. A., & Gordon, B. (2001) · Neurology · doi:10.1212/wnl.57.11.2045 · Cited by 301 · see citing works
Calford, M. B., & Aitkin, L. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-11-02365.1983 · Cited by 281 · see citing works
Comparative Studies on Vocalization in Marmoset Monkeys (Hapalidae)
Epple, G. (1968) · Folia Primatologica · doi:10.1159/000155129 · Cited by 280 · see citing works
Suppressed Responses to Self-triggered Sounds in the Human Auditory Cortex
Martikainen, M. H. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh131 · Cited by 274 · see citing works
Li, L., Lu, T., & Wang, X. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.87.5.2237 · Cited by 267 · see citing works
Self-citationGracco, V., & Abbs, J. H. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.54.2.418 · Cited by 263 · see citing works
Paus, T., Perry, D. W., Zatorre, R. J., Worsley, K. J., & Evans, A. C. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01187.x · Cited by 262 · see citing works
Independent control of human finger‐tip forces at individual digits during precision lifting.
Edin, B. B., Westling, G., & Johansson, R. S. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019142 · Cited by 240 · see citing works
Selective Vocal Effects Of Delayed Auditory Feedback
Fairbanks, G. (1955) · Journal of Speech and Hearing Disorders · doi:10.1044/jshd.2004.333 · Cited by 228 · see citing works
Neuronal activity in the human lateral temporal lobe
Creutzfeldt, O. D., Ojemann, G. A., & Lettich, E. (1989) · Experimental Brain Research · doi:10.1007/bf00249601 · Cited by 226 · see citing works
Inhibition of auditory cortical neurons during phonation
̈ller-Preuss, P. M., & Ploog, D. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)90491-1 · Cited by 215 · see citing works
Subdivisions and connections of auditory cortex in owl monkeys
Morel, A., & Kaas, J. H. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903180104 · Cited by 214 · see citing works
Kusunoki, M., & Goldberg, M. E. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00519.2002 · Cited by 211 · see citing works
Vision During Saccadic Eye Movements
Binda, P., & Morrone, M. C. (2018) · Annual Review of Vision Science · doi:10.1146/annurev-vision-091517-034317 · Cited by 191 · see citing works
Amplitude regulation of vocalizations in noise by a songbird,Taeniopygia guttata
Cynx, J., LEWIS, R., TAVEL, B., & TSE, H. (1998) · Animal Behaviour · doi:10.1006/anbe.1998.0746 · Cited by 185 · see citing works
ACOUSTIC AND NONACOUSTIC FACTORS MODIFYING MIDDLE-EAR MUSCLE ACTIVITY IN WAKING CATS
Carmel, P. W., & Starr, A. (1963) · Journal of Neurophysiology · doi:10.1152/jn.1963.26.4.598 · Cited by 175 · see citing works
On cortical coding of vocal communication sounds in primates
Wang, X. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.22.11843 · Cited by 175 · see citing works
Self-citationThe activity and function of the middle‐ear muscles in echo‐locating bats.
Henson, O. W. (1965) · The Journal of Physiology · doi:10.1113/jphysiol.1965.sp007737 · Cited by 169 · see citing works
Neural Representations of Temporally Asymmetric Stimuli in the Auditory Cortex of Awake Primates
Lu, T., Li, L., & Wang, X. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.6.2364 · Cited by 167 · see citing works
Self-citationSubject's own speech reduces reactivity of the human auditory cortex
Numminen, J., Salmelin, R., & Hari, R. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00218-9 · Cited by 163 · see citing works
Kadia, S. C., & Wang, X. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00271.2001 · Cited by 159 · see citing works
Self-citationResponse to frequency shifted artificial echoes in the batRhinolophus ferrumequinum
Schuller, G., Beuter, K., & Schnitzler, H. U. (1974) · Journal of Comparative Physiology A · doi:10.1007/bf00696191 · Cited by 142 · see citing works
Vision during saccadic eye movements. I. Visual interactions in striate cortex
Judge, S. J., Wurtz, R. H., & Richmond, B. J. (1980) · Journal of Neurophysiology · doi:10.1152/jn.1980.43.4.1133 · Cited by 139 · see citing works
Peripheral control of acoustic signals in the auditory system of echolocating bats
Suga, N., & Jen, P. H.-S. (1975) · Journal of Experimental Biology · doi:10.1242/jeb.62.2.277 · Cited by 135 · see citing works
Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs
Abeles, M., & Goldstein, M. H. (1972) · Brain Research · doi:10.1016/0006-8993(72)90535-5 · Cited by 129 · see citing works
Sensory coding and corollary discharge effects in mormyrid electric fish
Bell, C. C. (1989) · Journal of Experimental Biology · doi:10.1242/jeb.146.1.229 · Cited by 128 · see citing works
Regulation of voice amplitude by the monkey
Sinnott, J. M., Stebbins, W. C., & Moody, D. B. (1975) · The Journal of the Acoustical Society of America · doi:10.1121/1.380685 · Cited by 117 · see citing works
Auditory cortico‐cortical connections in the owl monkey
FitzPatrick, K. A., & Imig, T. J. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901920314 · Cited by 115 · see citing works
Kuwada, S., & Batra, R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-06-02273.1999 · Cited by 114 · see citing works
Site of Neural Attenuation of Responses to Self-Vocalized Sounds in Echolocating Bats
Suga, N., & Shimozawa, T. (1974) · Science · doi:10.1126/science.183.4130.1211 · Cited by 109 · see citing works
Auditory feedback in the regulation of voice
Siegel, G. M., & Pick, H. L. (1974) · The Journal of the Acoustical Society of America · doi:10.1121/1.1903486 · Cited by 90 · see citing works
Lombard reflex during PAG-induced vocalization in decerebrate cats
Nonaka, S., Takahashi, R., Enomoto, K., Katada, A., & Unno, T. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(97)00097-7 · Cited by 76 · see citing works
A possible neuronal basis for Doppler-shift compensation in echo-locating horseshoe bats
Metzner, W. (1989) · Nature · doi:10.1038/341529a0 · Cited by 59 · see citing works
Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey
Kirzinger, A., & J�rgens, U. (1991) · Experimental Brain Research · doi:10.1007/bf00230967 · Cited by 57 · see citing works
The effect of visuomotor displacements on arm movement paths
Goodbody, S. J., & Wolpert, D. M. (1999) · Experimental Brain Research · doi:10.1007/s002210050791 · Cited by 54 · see citing works
Harderian Gland: Influence on Pineal Hydroxyindole- O -Methyltransferase Activity in Neonatal Rats
Wetterberg, L., Yuwiler, A., Ulrich, R., et al. (1970) · Science · doi:10.1126/science.170.3954.194 · Cited by 44 · see citing works
Audition and the auditory pathway of a vocal new world primate, the common marmoset
Aitkin, L., & Park, V. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90004-c · Cited by 43 · see citing works
A Corollary Discharge Mechanism Modulates Central Auditory Processing in Singing Crickets
Poulet, J. F. A., & Hedwig, B. (2003) · Journal of Neurophysiology · doi:10.1152/jn.0846.2002 · Cited by 41 · see citing works
A Neural Basis for Auditory Feedback Control of Vocal Pitch
Smotherman, M. S., Zhang, S., & Metzner, W. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01464.2003 · Cited by 39 · see citing works
Tammer, R., Ehrenreich, L., & Jürgens, U. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.008 · Cited by 30 · see citing works
Auditory response following vocalization: a magnetoencephalographic study
Gunji, A., Hoshiyama, M., & Kakigi, R. (2001) · Clinical Neurophysiology · doi:10.1016/s1388-2457(01)00462-x · Cited by 27 · see citing works
SCHMOLESKY, M. T., Wang, Y., Creel, D. J., & Leventhal, A. G. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001113)427:2 · Cited by 13 · see citing works
Curio (2000) · doi:10.1002/(sici)1097-0193(200004)9:4
Merchenthaler (1999) · doi:10.1002/(sici)1096-9861(19990111)403:2
Flagged first, then by citations
Cited by
Sorted by citations
Corollary discharge across the animal kingdom
Crapse, T. B., & Sommer, M. A. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2457 · Cited by 789 · see citing works
The DIVA model: A neural theory of speech acquisition and production
Tourville, J. A., & Guenther, F. H. (2011) · Language and Cognitive Processes · doi:10.1080/01690960903498424 · Cited by 748 · see citing works
“…of auditory response suppression during self-initiated vocalisations is provided by single unit recordings from non-human primates; for example, attenuation of auditory cortical responses prior to self-initiated vocalisations has been demonstrated in the marmoset (Eliades & Wang, 2003, 2005).”
Neural mechanisms underlying auditory feedback control of speech
Tourville, J. A., Reilly, K. J., & Guenther, F. H. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.09.054 · Cited by 649 · see citing works
Neural substrates of vocalization feedback monitoring in primate auditory cortex
Eliades, S. J., & Wang, X. (2008) · Nature · doi:10.1038/nature06910 · Cited by 479 · see citing works
Self-citationSpeech Production as State Feedback Control
Houde, J. F., & Nagarajan, S. S. (2011) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2011.00082 · Cited by 463 · see citing works
Zheng, Z. Z., Munhall, K. G., & Johnsrude, I. S. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21324 · Cited by 177 · see citing works
Tian, X., & Poeppel, D. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00314 · Cited by 161 · see citing works
Error-dependent modulation of speech-induced auditory suppression for pitch-shifted voice feedback
Behroozmand, R., & Larson, C. R. (2011) · BMC Neuroscience · doi:10.1186/1471-2202-12-54 · Cited by 158 · see citing works
Speech target modulates speaking induced suppression in auditory cortex
Ventura, M. I., Nagarajan, S. S., & Houde, J. F. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-58 · Cited by 113 · see citing works
Anticipating the future: Automatic prediction failures in schizophrenia
Ford, J. M., & Mathalon, D. H. (2012) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2011.09.004 · Cited by 113 · see citing works
Modeling the Role of Sensory Feedback in Speech Motor Control and Learning
Parrell, B., & Houde, J. (2019) · Journal of Speech, Language, and Hearing Research · doi:10.1044/2019_jslhr-s-csmc7-18-0127 · Cited by 75 · see citing works
Christoffels, I. K., van de Ven, V., Waldorp, L. J., Formisano, E., & Schiller, N. O. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018307 · Cited by 72 · see citing works
van de Ven, V., Esposito, F., & Christoffels, I. K. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.057 · Cited by 72 · see citing works
Corollary Discharge Dysfunction in Schizophrenia: Evidence for an Elemental Deficit
Mathalon, D. H., & Ford, J. M. (2008) · Clinical EEG and Neuroscience · doi:10.1177/155005940803900212 · Cited by 60 · see citing works
- Authors
- Eliades, S. J., & Wang, X.
- Affiliations
- Johns Hopkins University (US)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-02-02
- Volume
- 15
- Issue
- 10
- Pages
- 1510-1523
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2128125220
- Cited by
- 150
- References
- 72
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 7 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 12 · 2019: 5 · 2018: 13 · 2017: 7 · 2016: 6 · 2015: 6 · 2014: 5 · 2013: 10 · 2012: 19
- FWCI
- 4.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (DC 005808, R01DC005808)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Phonetics and Phonology Research
- Keywords
- auditory cortex, single-unit activity, neuronal synchronization
- MeSH terms
- Acoustic Stimulation, Action Potentials, Animals, Auditory Cortex, Auditory Perception, Brain Mapping, Callithrix, Electrophysiology, Microelectrodes, Motor Neurons, Neurons, Vocalization, Animal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review