1932

Abstract

Hearing is often viewed as a passive process: Sound enters the ear, triggers a cascade of activity through the auditory system, and culminates in an auditory percept. In contrast to a passive process, motor-related signals strongly modulate the auditory system from the eardrum to the cortex. The motor modulation of auditory activity is most well documented during speech and other vocalizations but also can be detected during a wide variety of other sound-generating behaviors. An influential idea is that these motor-related signals suppress neural responses to predictable movement-generated sounds, thereby enhancing sensitivity to environmental sounds during movement while helping to detect errors in learned acoustic behaviors, including speech and musicianship. Findings in humans, monkeys, songbirds, and mice provide new insights into the circuits that convey motor-related signals to the auditory system, while lending support to the idea that these signals function predictively to facilitate hearing and vocal learning.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-072116-031215
2018-07-08
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/neuro/41/1/annurev-neuro-072116-031215.html?itemId=/content/journals/10.1146/annurev-neuro-072116-031215&mimeType=html&fmt=ahah

Literature Cited

  1. Akutagawa E, Konishi M 2010. New brain pathways found in the vocal control system of a songbird. J. Comp. Neurol. 518:3086–100
    [Google Scholar]
  2. Alexander GE, Newman JD, Symmes D 1976. Convergence of prefrontal and acoustic inputs upon neurons in the superior temporal gyrus of the awake squirrel monkey. Brain Res 116:334–38
    [Google Scholar]
  3. Andalman AS, Fee MS 2009. A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors. PNAS 106:12518–23
    [Google Scholar]
  4. Aronov D, Andalman AS, Fee MS 2008. A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320:630–34
    [Google Scholar]
  5. Bao S, Chan VT, Merzenich MM 2001. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412:79–83
    [Google Scholar]
  6. Behroozmand R, Larson CR 2011. Error-dependent modulation of speech-induced auditory suppression for pitch-shifted voice feedback. BMC Neurosci 12:54
    [Google Scholar]
  7. Behroozmand R, Oya H, Nourski KV, Kawasaki H, Larson CR et al. 2016. Neural correlates of vocal production and motor control in human Heschl's gyrus. J. Neurosci. 36:2302–15
    [Google Scholar]
  8. Broca P 1861. Remarks on the seat of the faculty of articulate language, following an observation of aphemia (loss of speech). Bull. Soc. Anat. 6:330–57
    [Google Scholar]
  9. Canopoli A, Herbst JA, Hahnloser RH 2014. A higher sensory brain region is involved in reversing reinforcement-induced vocal changes in a songbird. J. Neurosci. 34:7018–26
    [Google Scholar]
  10. Carmel PW, Starr A 1964. Non-acoustic factors influencing activity of middle ear muscles in waking cats. Nature 202:195–96
    [Google Scholar]
  11. Creutzfeldt O, Ojemann G, Lettich E 1989. Neuronal activity in the human lateral temporal lobe. II. Responses to the subjects own voice. Exp. Brain Res. 77:476–89
    [Google Scholar]
  12. Curio G, Neuloh G, Numminen J, Jousmaki V, Hari R 2000. Speaking modifies voice-evoked activity in the human auditory cortex. Hum. Brain Mapp. 9:183–91
    [Google Scholar]
  13. Deacon TW 1992. Cortical connections of the inferior arcuate sulcus cortex in the macaque brain. Brain Res 573:8–26
    [Google Scholar]
  14. Doupe AJ, Kuhl PK 1999. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22:567–631
    [Google Scholar]
  15. Eliades SJ, Wang X 2003. Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. J. Neurophysiol. 89:2194–207
    [Google Scholar]
  16. Eliades SJ, Wang X 2005. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb. Cortex 15:1510–23
    [Google Scholar]
  17. Eliades SJ, Wang X 2008. Neural substrates of vocalization feedback monitoring in primate auditory cortex. Nature 453:1102–6
    [Google Scholar]
  18. Eliades SJ, Wang X 2017. Contributions of sensory tuning to auditory-vocal interactions in marmoset auditory cortex. Hear Res 348:98–111
    [Google Scholar]
  19. Flinker A, Chang EF, Kirsch HE, Barbaro NM, Crone NE, Knight RT 2010. Single-trial speech suppression of auditory cortex activity in humans. J. Neurosci. 30:16643–50
    [Google Scholar]
  20. Flinker A, Korzeniewska A, Shestyuk AY, Franaszczuk PJ, Dronkers NF et al. 2015. Redefining the role of Broca's area in speech. PNAS 112:2871–75
    [Google Scholar]
  21. Ford JM, Mathalon DH, Heinks T, Kalba S, Faustman WO, Roth WT 2001. Neurophysiological evidence of corollary discharge dysfunction in schizophrenia. Am. J. Psychiatry 158:2069–71
    [Google Scholar]
  22. Froemke RC, Merzenich MM, Schreiner CE 2007. A synaptic memory trace for cortical receptive field plasticity. Nature 450:425–29
    [Google Scholar]
  23. Gadagkar V, Puzerey PA, Chen R, Baird-Daniel E, Farhang AR, Goldberg JH 2016. Dopamine neurons encode performance error in singing birds. Science 354:1278–82
    [Google Scholar]
  24. Geschwind N, Levitsky W 1968. Human brain: left-right asymmetries in temporal speech region. Science 161:186–87
    [Google Scholar]
  25. Guenther FH, Hickok G 2015. Role of the auditory system in speech production. Handb. Clin. Neurol. 129:161–75
    [Google Scholar]
  26. Gutschalk A, Rupp A, Dykstra AR 2015. Interaction of streaming and attention in human auditory cortex. PLOS ONE 10:e0118962
    [Google Scholar]
  27. Hackett TA 2015. Anatomic organization of the auditory cortex. Handb. Clin. Neurol. 129:27–53
    [Google Scholar]
  28. Hackett TA, Stepniewska I, Kaas JH 1999. Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res 817:45–58
    [Google Scholar]
  29. Hahnloser RH, Kozhevnikov AA, Fee MS 2002. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65–70
    [Google Scholar]
  30. Hamaguchi K, Tanaka M, Mooney R 2016. A distributed recurrent network contributes to temporally precise vocalizations. Neuron 91:680–93
    [Google Scholar]
  31. Heinks-Maldonado TH, Mathalon DH, Gray M, Ford JM 2005. Fine-tuning of auditory cortex during speech production. Psychophysiology 42:180–90
    [Google Scholar]
  32. Hickok G 2012. Computational neuroanatomy of speech production. Nat. Rev. Neurosci. 13:135–45
    [Google Scholar]
  33. Hickok G, Poeppel D 2007. The cortical organization of speech processing. Nat. Rev. Neurosci. 8:393–402
    [Google Scholar]
  34. Hisey E, Kearney MG, Mooney R 2018. A common neural circuit for internally guided and externally reinforced forms of motor learning. Nat. Neurosci. 21:589–97
    [Google Scholar]
  35. Houde JF, Nagarajan SS, Sekihara K, Merzenich MM 2002. Modulation of the auditory cortex during speech: an MEG study. J. Cogn. Neurosci. 14:1125–38
    [Google Scholar]
  36. Keller GB, Hahnloser RH 2009. Neural processing of auditory feedback during vocal practice in a songbird. Nature 457:187–90
    [Google Scholar]
  37. Kilgard MP, Merzenich MM 1998. Plasticity of temporal information processing in the primary auditory cortex. Nat. Neurosci. 1:727–31
    [Google Scholar]
  38. Kuchibhotla KV, Gill JV, Lindsay GW, Papadoyannis ES, Field RE et al. 2017. Parallel processing by cortical inhibition enables context-dependent behavior. Nat. Neurosci. 20:62–71
    [Google Scholar]
  39. Lee SH, Dan Y 2012. Neuromodulation of brain states. Neuron 76:209–22
    [Google Scholar]
  40. Lehmann J, Nagy JI, Atmadia S, Fibiger HC 1980. The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat. Neuroscience 5:1161–74
    [Google Scholar]
  41. Leichnetz GR, Astruc J 1975. Efferent connections of the orbitofrontal cortex in the marmoset (Saguinus oedipus). Brain Res 84:169–80
    [Google Scholar]
  42. Lienweber M, Ward D, Sobczak J, Attinger A, Keller GB 2017. A sensorimotor circuit in mouse cortex for visual flow predictions. Neuron 95:1420–32
    [Google Scholar]
  43. Long MA, Fee MS 2008. Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456:189–94
    [Google Scholar]
  44. Long MA, Katlowitz KA, Svirsky MA, Clary RC, Byun TM et al. 2016. Functional segregation of cortical regions underlying speech timing and articulation. Neuron 89:1187–93
    [Google Scholar]
  45. Lynch GF, Okubo TS, Hanuschkin A, Hahnloser RH, Fee MS 2016. Rhythmic continuous-time coding in the songbird analog of vocal motor cortex. Neuron 90:877–92
    [Google Scholar]
  46. Mahrt EJ, Perkel DJ, Tong L, Rubel EW, Portfors CV 2013. Engineered deafness reveals that mouse courtship vocalizations do not require auditory experience. J. Neurosci. 33:5573–83
    [Google Scholar]
  47. Mandelblat-Cerf Y, Las L, Denisenko N, Fee MS 2014. A role for descending auditory cortical projections in songbird vocal learning. eLife 3:e04371
    [Google Scholar]
  48. Marr D 1982. Vision Cambridge, MA: MIT Press
  49. McGinley MJ, David SV, McCormick DA 2015a. Cortical membrane potential signature of optimal states for sensory signal detection. Neuron 87:179–92
    [Google Scholar]
  50. McGinley MJ, Vinck M, Reimer J, Batista-Brito R, Zagha E et al. 2015b. Waking state: Rapid variations modulate neural and behavioral responses. Neuron 87:1143–61
    [Google Scholar]
  51. Mehl MR, Vazire S, Ramirez-Esparza N, Slatcher RB, Pennebaker JW 2007. Are women really more talkative than men. Science 317:82
    [Google Scholar]
  52. Morel A, Garraghty PE, Kaas JH 1993. Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. J. Comp. Neurol. 335:437–59
    [Google Scholar]
  53. Möttönen R, Watkins K 2009. Motor representations of articulators contribute to categorical perception of speech sounds. J. Neurosci. 29:9819–25
    [Google Scholar]
  54. Mukerji S, Windsor AM, Lee DJ 2010. Auditory brainstem circuits that mediate the middle ear muscle reflex. Trends Amplif 14:170–91
    [Google Scholar]
  55. Müller-Preuss P, Ploog D 1981. Inhibition of auditory cortical neurons during phonation. Brain Res 215:61–76
    [Google Scholar]
  56. Nelson A, Mooney R 2016. The basal forebrain and motor cortex provide convergent yet distinct movement-related inputs to the auditory cortex. Neuron 90:635–48
    [Google Scholar]
  57. Nelson A, Schneider DM, Takatoh J, Sakurai K, Wang F, Mooney R 2013. A circuit for motor cortical modulation of auditory cortical activity. J. Neurosci. 33:14342–53
    [Google Scholar]
  58. Niell CM, Stryker MP 2010. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65:472–79
    [Google Scholar]
  59. Niziolek CA, Nagarajan SS, Houde JF 2013. What does motor efference copy represent? Evidence from speech production. J. Neurosci. 33:16110–16
    [Google Scholar]
  60. Nottebohm F, Kelley DB, Paton JA 1982. Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207:344–57
    [Google Scholar]
  61. Nottebohm F, Stokes TM, Leonard CM 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165:457–86
    [Google Scholar]
  62. Numminen J, Curio G 1999. Differential effects of overt, covert and replayed speech on vowel-evoked responses of the human auditory cortex. Neurosci. Lett. 272:29–32
    [Google Scholar]
  63. Ojemann GA 1991. Cortical organization of language. J. Neurosci. 11:2281–87
    [Google Scholar]
  64. Pasley BN, David SV, Mesgarani N, Flinker A, Shamma SA et al. 2012. Reconstructing speech from human auditory cortex. PLOS Biol 10:e1001251
    [Google Scholar]
  65. Peretz I, Kolinsky R, Tramo M, Labrecque R, Hublet C et al. 1994. Functional dissociations following bilateral lesions of auditory cortex. Brain 117:Pt. 61283–301
    [Google Scholar]
  66. Petrides M, Pandya DN 1988. Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J. Comp. Neurol. 273:52–66
    [Google Scholar]
  67. Petrides M, Pandya DN 2002. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur. J. Neurosci. 16:291–310
    [Google Scholar]
  68. Picardo MA, Merel J, Katlowitz KA, Vallentin D, Okobi DE et al. 2016. Population-level representation of a temporal sequence underlying song production in the zebra finch. Neuron 90:866–76
    [Google Scholar]
  69. Portfors CV 2007. Types and functions of ultrasonic vocalizations in laboratory rats and mice. J. Am. Assoc. Lab. Anim. Sci. 46:28–34
    [Google Scholar]
  70. Poulet JF, Hedwig B 2002. A corollary discharge maintains auditory sensitivity during sound production. Nature 418:872–76
    [Google Scholar]
  71. Prather JF, Peters S, Nowicki S, Mooney R 2008. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451:305–10
    [Google Scholar]
  72. Prather JF, Peters S, Nowicki S, Mooney R 2010. Persistent representation of juvenile experience in the adult songbird brain. J. Neurosci. 31:10586–98
    [Google Scholar]
  73. Rauschecker JP, Scott SK 2009. Maps and streams in the auditory cortex: Nonhuman primates illuminate human speech processing. Nat. Neurosci. 12:718–24
    [Google Scholar]
  74. Reimer J, Froudarakis E, Cadwell CR, Yatsenko D, Denfield GH, Tolias AS 2014. Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 84:355–62
    [Google Scholar]
  75. Reznik D, Henkin Y, Schadel N, Mukamel R 2014. Lateralized enhancement of auditory cortex activity and increased sensitivity to self-generated sounds. Nat. Commun. 5:4059
    [Google Scholar]
  76. Reznik D, Ossmy O, Mukamel R 2015. Enhanced auditory evoked activity to self-generated sounds is mediated by primary and supplementary motor cortices. J. Neurosci. 35:2173–80
    [Google Scholar]
  77. Roberts TF, Gobes SM, Murugan M, Olevczky BP, Mooney R 2012. Rapid spine stabilization and synaptic enhancement at the onset of behavioral learning. Nat. Neurosci. 15:1454–59
    [Google Scholar]
  78. Roberts TF, Hisey E, Tanaka M, Kearney MG, Chattree G et al. 2017. Identification of a motor-to-auditory pathway important for vocal learning. Nat. Neurosci. 20:978–86
    [Google Scholar]
  79. Roberts TF, Tschida KA, Klein ME, Mooney R 2010. Rapid spine stabilization and synaptic enhancement at the onset of behavioral learning. Nature 463:948–52
    [Google Scholar]
  80. Romanski LM, Averbeck BB 2009. The primate cortical auditory system and neural representation of conspecific vocalizations. Annu. Rev. Neurosci. 32:315–46
    [Google Scholar]
  81. Romanski LM, Bates JF, Goldman-Rakic PS 1999. Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 403:141–57
    [Google Scholar]
  82. Rummell BP, Klee JL, Sigurdsson T 2016. Attenuation of responses to self-generated sounds in auditory cortical neurons. J. Neurosci. 36:12010–26
    [Google Scholar]
  83. Salomon G, Starr A 1963. Sound sensations arising from direct current stimulation of the cochlea in man. Dan. Med. Bull. 10:215–16
    [Google Scholar]
  84. Schneider DM, Mooney R 2017. Motor cortex suppresses auditory cortical responses to self-generated sounds Presented at Soc. Neurosci. Nov. 11–15 Washington, DC:
  85. Schneider DM, Nelson A, Mooney R 2014. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513:189–94
    [Google Scholar]
  86. Scott SK, Johnsrude IS 2003. The neuroanatomical and functional organization of speech perception. Trends Neurosci 26:100–7
    [Google Scholar]
  87. Sheppard JP, Raposo D, Churchland AK 2013. Dynamic reweighting of multisensory stimuli shapes decision-making in rats and humans. J. Vis. 13:1–19
    [Google Scholar]
  88. Singla S, Dempsey C, Warren R, Enikolopov AG, Sawtell NB 2017. A cerebellum-like circuit in the auditory system cancels responses to self-generated sounds. Nat. Neurosci. 20:943–50
    [Google Scholar]
  89. Sober SJ, Brainard MS 2009. Adult birdsong is actively maintained by error correction. Nat. Neurosci. 12:927–31
    [Google Scholar]
  90. Sperry RW 1950. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43:482–89
    [Google Scholar]
  91. Stenner MP, Bauer M, Heinze HJ, Haggard P, Dolan RJ 2015. Parallel processing streams for motor output and sensory prediction during action preparation. J. Neurophysiol. 113:1752–62
    [Google Scholar]
  92. Stewart L, von Kriegstein K, Warren JD, Griffiths TD 2006. Music and the brain: disorders of musical listening. Brain 129:Pt. 102533–53
    [Google Scholar]
  93. Suga N, Shimozawa T 1974. Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science 183:1211–13
    [Google Scholar]
  94. Sundararajan J, Schneider DM, Mooney R 2017. Mechanisms of movement-related changes to auditory detection thresholds Presented at Soc. Neurosci. Nov. 11–15 Washington, DC:
  95. Tian X, Poeppel D 2010. Mental imagery of speech and movement implicates the dynamics of internal forward models. Front. Psychol. 1:166
    [Google Scholar]
  96. Timm J, Schönwiesner M, Schröger E, SanMiguel I 2016. Sensory suppression of brain responses to self-generated sounds is observed with and without the perception of agency. Cortex 80:5–20
    [Google Scholar]
  97. Tumer E, Brainard M 2007. Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong. Nature 450:1240–44
    [Google Scholar]
  98. Vallentin D, Kosche G, Lipkind D, Long MA 2016. Inhibition protects acquired song segments during vocal learning in zebra finches. Science 351:267–71
    [Google Scholar]
  99. van Elk M, Lenggenhager B, Heydrich L, Blanke O 2014. Suppression of the auditory N1-component for heartbeat-related sounds reflects interoceptive predictive coding. Biol. Psychol. 99:172–82
    [Google Scholar]
  100. von Holst E, Mittelstaedt H 1950. The reafference principle. Interaction between the central nervous system and the periphery. Selected Papers of Erich von Holst: The Behavioural Physiology of Animals and Man 139–73 London: Methuen (from German)
    [Google Scholar]
  101. Weiss C, Herwig A, Schütz-Bosbach S 2011. The self in action effects: selective attenuation of self-generated sounds. Cognition 121:207–18
    [Google Scholar]
  102. Wolpert DM, Ghahramani Z, Jordan MI 1995. An internal model for sensorimotor integration. Science 269:1880–82
    [Google Scholar]
  103. Woolley SM, Rubel EW 1997. Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song. J. Neurosci. 17:6380–90
    [Google Scholar]
  104. Zatorre RJ 1988. Pitch perception of complex tones and human temporal-lobe function. J. Acoust. Soc. Am. 84:566–72
    [Google Scholar]
  105. Zatorre RJ 2007. There's more to auditory cortex than meets the ear. Hear Res 229:24–30
    [Google Scholar]
  106. Zatorre RJ, Belin P, Penhune VB 2002. Structure and function of auditory cortex: music and speech. Trends Cogn. Sci. 6:37–46
    [Google Scholar]
  107. Zhou M, Liang F, Xiong XR, Li L, Li H et al. 2014. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17:841–50
    [Google Scholar]
  108. Zmarz P, Keller GB 2016. Mismatch receptive fields in mouse visual cortex. Neuron 92:766–72
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-072116-031215
Loading
/content/journals/10.1146/annurev-neuro-072116-031215
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error