The Brain Bases of Phantom Auditory Phenomena: From Tinnitus to Hearing Voices

Abstract

The phenomenology and neural bases of phantom auditory perceptions are reviewed. A variety of phantom auditory phenomena are discussed, from tinnitus to hearing voices. It is claimed that the phenomenology or qualia of the hallucinatory experience may correspond to how the auditory system is organized into functional regions (neural architecture) and how auditory percepts are represented at the single neuron level within this system. There may be a one-to-one correspondence between the type of experience (e.g., hearing a tone versus hearing a voice) and the representational qualities or aspects of sound representation in different parts of the auditory and speech processing stream or system. The literature does not support the supposition that certain features of auditory hallucinations correspond to either neurological or psychiatric disease. Clinical aspects of auditory hallucinations also are discussed that may be of interest to clinical practitioners with patients who have auditory hallucinations.

Keywords

auditory hallucinations - tinnitus - music hallucinations - voices - schizophrenia

• References

• 1 Folmer RL, Griest SE, Martin WH. Chronic tinnitus as phantom auditory pain. Otolaryngol Head Neck Surg 2001; 124: 394-400
• 2 Demeester K, van Wieringen A, Hendrickx JJ , et al. Prevalence of tinnitus and audiometric shape. B-ENT 2007; 3 (Suppl. 07) 37-49
• 3 David AS. The cognitive neuropsychiatry of auditory verbal hallucinations: an overview. Cogn Neuropsychiatry 2004; 9: 107-123
• 4 Hug A, Bartsch A, Gutschalk A. Voices behind the left shoulder: two patients with right-sided temporal lobe epilepsy. J Neurol Sci 2011; 305: 143-146
• 5 Moskowitz A, Heim G. Eugen Bleuler's dementia praecox or the group of schizophrenias (1911): a centenary appreciation and reconsideration. Schizophr Bull 2011; 37: 471-479
• 6 Silbersweig D, Stern E. Functional neuroimaging of hallucinations in schizophrenia: toward an integration of bottom-up and top-down approaches. Mol Psychiatry 1996; 1: 367-375
• 7 Ohayon MM, Priest RG, Caulet M, Guilleminault C. Hypnagogic and hypnopompic hallucinations: pathological phenomena?. Br J Psychiatry 1996; 169: 459-467
• 8 Cockshutt G. Choices for voices: a voice hearer's perspective on hearing voices. Cogn Neuropsychiatry 2004; 9: 9-11
• 9 Peroutka SJ, Sohmer BH, Kumar AJ, Folstein M, Robinson RG. Hallucinations and delusions following a right temporoparietooccipital infarction. Johns Hopkins Med J 1982; 151: 181-185
• 10 Ffytche DH, Howard RJ, Brammer MJ, David A, Woodruff P, Williams S. The anatomy of conscious vision: an fMRI study of visual hallucinations. Nat Neurosci 1998; 1: 738-742
• 11 Santhouse AM, Howard RJ, ffytche DH. Visual hallucinatory syndromes and the anatomy of the visual brain. Brain 2000; 123 (Pt 10) 2055-2064
• 12 Formisano E, Kim DS, Di Salle F, van de Moortele PF, Ugurbil K, Goebel R. Mirror-symmetric tonotopic maps in human primary auditory cortex. Neuron 2003; 40: 859-869
• 13 Yang S, Weiner BD, Zhang LS, Cho SJ, Bao S. Homeostatic plasticity drives tinnitus perception in an animal model. Proc Natl Acad Sci U S A 2011; 108: 14974-14979
• 14 Mühlnickel W, Elbert T, Taub E, Flor H. Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci U S A 1998; 95: 10340-10343
• 15 De Ridder D, De Mulder G, Walsh V, Muggleton N, Sunaert S, Møller A. Magnetic and electrical stimulation of the auditory cortex for intractable tinnitus. Case report. J Neurosurg 2004; 100: 560-564
• 16 Rauschecker JP, Leaver AM, Mühlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 2010; 66: 819-826
• 17 Hickok G, Poeppel D. Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition 2004; 92: 67-99
• 18 Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci 2007; 8: 393-402
• 19 Kriegstein KV, Giraud AL. Distinct functional substrates along the right superior temporal sulcus for the processing of voices. Neuroimage 2004; 22: 948-955
• 20 Pelphrey KA, Morris JP, Michelich CR, Allison T, McCarthy G. Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. Cereb Cortex 2005; 15: 1866-1876
• 21 Baron-Cohen S, Wheelwright S, Jolliffe T. Is there a “language of the eyes”? Evidence from normal adults, and adults with autism or Asperger syndrome. Vis Cogn 1997; 4: 311-331
• 22 Decety J, Lamm C. The role of the right temporoparietal junction in social interaction: how low-level computational processes contribute to meta-cognition. Neuroscientist 2007; 13: 580-593
• 23 Puce A, Perrett D. Electrophysiology and brain imaging of biological motion. Philos Trans R Soc Lond B Biol Sci 2003; 358: 435-445
• 24 Redcay E. The superior temporal sulcus performs a common function for social and speech perception: implications for the emergence of autism. Neurosci Biobehav Rev 2008; 32: 123-142
• 25 Saxe R, Wexler A. Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia 2005; 43: 1391-1399
• 26 Wible CG, Preus AP, Hashimoto R. A cognitive neuroscience view of schizophrenic symptoms: abnormal activation of a system for social perception and communication. Brain Imaging Behav 2009; 3: 85-110
• 27 Wible CG. Hippocampal Temporal-Parietal Junction Interaction in the Production of Psychotic Symptoms: A Framework for Understanding the Schizophrenic Syndrome. Frontiers in Neuroscience ; In press
• 28 Jellema T, Baker CI, Wicker B, Perrett DI. Neural representation for the perception of the intentionality of actions. Brain Cogn 2000; 44: 280-302
• 29 Morris JP, Pelphrey KA, McCarthy G. Perceived causality influences brain activity evoked by biological motion. Soc Neurosci 2008; 3: 16-25
• 30 Blanke O, Ortigue S, Landis T, Seeck M. Stimulating illusory own-body perceptions. Nature 2002; 419: 269-270
• 31 Ghazanfar AA, Chandrasekaran C, Logothetis NK. Interactions between the superior temporal sulcus and auditory cortex mediate dynamic face/voice integration in rhesus monkeys. J Neurosci 2008; 28: 4457-4469
• 32 Ditman T, Kuperberg GR. Building coherence: a framework for exploring the breakdown of links across clause boundaries in schizophrenia. J Neurolinguist 2010; 23: 254-269
• 33 Redcay E, Dodell-Feder D, Pearrow MJ , et al. Live face-to-face interaction during fMRI: a new tool for social cognitive neuroscience. Neuroimage 2010; 50: 1639-1647
• 34 Nummenmaa L, Passamonti L, Rowe J, Engell AD, Calder AJ. Connectivity analysis reveals a cortical network for eye gaze perception. Cereb Cortex 2010; 20: 1780-1787
• 35 Wright TM, Pelphrey KA, Allison T, McKeown MJ, McCarthy G. Polysensory interactions along lateral temporal regions evoked by audiovisual speech. Cereb Cortex 2003; 13: 1034-1043
• 36 Blanke O, Arzy S. The out-of-body experience: disturbed self-processing at the temporo-parietal junction. Neuroscientist 2005; 11: 16-24
• 37 Young L, Dodell-Feder D, Saxe R. What gets the attention of the temporo-parietal junction? An fMRI investigation of attention and theory of mind. Neuropsychologia 2010; 48: 2658-2664
• 38 Adolphs R, Damasio H, Tranel D. Neural systems for recognition of emotional prosody: a 3-D lesion study. Emotion 2002; 2: 23-51
• 39 Lennox BR, Park SB, Jones PB, Morris PG. Spatial and temporal mapping of neural activity associated with auditory hallucinations. Lancet 1999; 353: 644
• 40 Allen P, Larøi F, McGuire PK, Aleman A. The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci Biobehav Rev 2008; 32: 175-191
• 41 Hoffman RE, Gueorguieva R, Hawkins KA , et al. Temporoparietal transcranial magnetic stimulation for auditory hallucinations: safety, efficacy and moderators in a fifty patient sample. Biol Psychiatry 2005; 58: 97-104
• 42 Rogalsky C, Rong F, Saberi K, Hickok G. Functional anatomy of language and music perception: temporal and structural factors investigated using functional magnetic resonance imaging. J Neurosci 2011; 31: 3843-3852
• 43 Peretz I, Gosselin N, Belin P, Zatorre RJ, Plailly J, Tillmann B. Music lexical networks: the cortical organization of music recognition. Ann N Y Acad Sci 2009; 1169: 256-265
• 44 Cope TE, Baguley DM. Is musical hallucination an otological phenomenon? A review of the literature. Clin Otolaryngol 2009; 34: 423-430
• 45 Isolan GR, Bianchin MM, Bragatti JA, Torres C, Schwartsmann G. Musical hallucinations following insular glioma resection. Neurosurg Focus 2010; 28: E9
• 46 Mori T, Ikeda M, Fukuhara R , et al. Regional cerebral blood flow change in a case of Alzheimer's disease with musical hallucinations. Eur Arch Psychiatry Clin Neurosci 2006; 256: 236-239
• 47 Griffiths TD. Musical hallucinosis in acquired deafness. Phenomenology and brain substrate. Brain 2000; 123 (Pt 10) 2065-2076
• 48 Sacks O. Musicophilia: Tales of Music and the Brain. New York, NY: Alfred A. Knopf; 2007
• 49 Cole MG, Dowson L, Dendukuri N, Belzile E. The prevalence and phenomenology of auditory hallucinations among elderly subjects attending an audiology clinic. Int J Geriatr Psychiatry 2002; 17: 444-452
• 50 Coffey M, Hewitt J. “You don't talk about the voices”: voice hearers and community mental health nurses talk about responding to voice hearing experiences. J Clin Nurs 2008; 17: 1591-1600
• 51 Buccheri RK, Trygstad LN, Buffum MD, Lyttle K, Dowling G. Comprehensive evidence-based program teaching self-management of auditory hallucinations on inpatient psychiatric units. Issues Ment Health Nurs 2010; 31: 223-231