Current Controversies on Wernicke’s Area and its Role in Language

DeWitt I, Rauschecker JP. Wernicke’s area revisited: parallel streams and word processing. Brain Lang. 2013;127(2):181–91. Binder JR. The Wernicke area: modern evidence and a reinterpretation. Neurology. 2015;85:2170–5. • Mesulam MM, Thompson CK, Weintraub S, Rogalski EJ. The Wernicke conundrum and the anatomy of language comprehension in primary progressive aphasia. Brain. 2015;138(8):2423–37. This study uses data from a large cohort of patients with primary progressive aphasia to examine the neural correlates of language comprehension, concluding that word comprehension depends mainly on the left anterior temporal lobe. • Tremblay P, Dick AS. Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain Lang. 2016;162:60–71. This paper presents interesting survey data on current use of the terms Broca's area and Wernicke's area among language scientists and clinicians, and argues that a lack of agreement renders these terms largely meaningless. Wernicke C. Der aphasische Symptomenkomplex. Cohn & Weigert: Breslau; 1874. Lichtheim L. On aphasia. Brain. 1885;7:433–84. Henschen SE. On the hearing sphere. Acta Otolaryngol (Stockh). 1918-1919;1:423–86. Bastian HC. On different kinds of aphasia, with special reference to their classification and ultimate pathology. Br Med J. 1887;2:931–6. 85-90 Déjerine J. Anatomie des centres nerveux. Paris: Rueff; 1895. Pick A. Aphasia. Berlin: Springer; 1931. Kleist K. Sensory aphasia and amusia. London: Pergamon Press; 1962. Starr MA. The pathology of sensory aphasia, with an analysis of fifty cases in which Broca’s centre was not diseased. Brain. 1889;12:82–101. Marie P. On aphasia in general and agraphia in particular according to the teaching of Professor Charcot. Reprinted from Le Progres Medical, Series 2, 1888; 7: 81-84. Pierre Marie's Papers on Speech Disorders. New York: Hafner; 1971. Goldstein K. Language and language disturbances. New York: Grune & Stratton; 1948. Penfield W, Roberts L. Speech and brain-mechanisms. New York: Atheneum; 1959. Bogen JE, Bogen GM. Wernicke’s region—where is it? Ann N Y Acad Sci. 1976;290:834–43. Geschwind N. Aphasia. N Engl J Med. 1971;284(12):654–6. Geschwind N, Levitsky W. Human brain: left-right asymmetries in temporal speech region. Science. 1968;161:186–7. Wada JA, Clarke R, Hamm A. Cerebral hemispheric asymmetry in humans. Arch Neurol. 1975;32:239–46. Steinmetz H, Volkmann J, Jäncke L, Freund H-J. Anatomical left-right asymmetry of language-related temporal cortex is different in left- and right-handers. Ann Neurol. 1991;29:315–9. Galaburda AM, LeMay M, Kemper T, Geschwind N. Right-left asymmetries in the brain. Structural differences between the hemispheres may underlie cerebral dominance. Science. 1978;199:852–6. Witelson SF, Kigar DL. Sylvian fissure morphology and asymmetry in men and women: bilateral differences in relation to handedness in men. J Comp Neurol. 1992;323:326–40. Foundas AL, Leonard CM, Gilmore R, et al. Planum temporale asymmetry and language dominance. Neuropsychologia. 1994;32:1225–31. Benson DF. Aphasia, alexia and agraphia. New York: Churchill Livingstone; 1979. Mayeux R, Kandel ER. Natural language, disorders of language, and other localizable disorders of cognitive function. In: Kandel ER, Schwartz J, editors. Principles of Neural Science. 2nd ed. New York: Elsevier Science Publishing Co.; 1985. p. 688–703. Mesulam MM. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol. 1990;28:597–613. Benson DF, Sheremata WA, Bouchard R, et al. Conduction aphasia. A clinicopathological study. Arch Neurol. 1973;28:339–46. Boller F. Destruction of Wernicke’s area without language disturbance. A fresh look at crossed aphasia. Neuropsychologia. 1973;11:243–6. Damasio H, Damasio AR. The anatomical basis of conduction aphasia. Brain. 1980;103:337–50. Palumbo CL, Alexander MP, Naeser MA. CT scan lesion sites associated with conduction aphasia. In: Kohn SE, editor. Conduction aphasia. Hillsdale, NJ: Lawrence Erlbaum; 1992. p. 51–75. Axer H, Keyserlingk AG, Berks G, Keyserlingk DF. Supra- and infrasylvian conduction aphasia. Brain Lang. 2001;76:317–31. Fridriksson J, Kjartansson O, Morgan PS, et al. Impaired speech repetition and left parietal lobe damage. J Neurosci. 2010;30:11057–61. • Buchsbaum BR, Baldo J, D’Esposito M, et al. Conduction aphasia, sensory-motor integration, and phonological short-term memory: an aggregate analysis of lesion and fMRI data. Brain Lang. 2011;119:119–28. This paper presents a multi-faceted review and meta-analysis of neuroimaging data regarding phonological processing. Anderson JM, Gilmore R, Roper S, et al. Conduction aphasia and the arcuate fasciculus: a reexamination of the Wernicke-Geschwind model. Brain Lang. 1999;70:1–12. Quigg M, Fountain NB. Conduction aphasia elicited by stimulation of the left posterior superior temporal gyrus. J Neurol Neurosurg Psychiatry. 1999;66:393–6. Corina DP, Loudermilk BC, Detwiler L, et al. Analysis of naming errors during cortical stimulation mapping: implications for models of language representation. Brain Lang. 2010;115:101–12. Roux FE, Durand JB, Jucla M, et al. Segregation of lexical and sub-lexical reading processes in the left perisylvian cortex. PLoS One. 2012;7(11):e50665. Levelt WJM. Speaking: from intention to articulation. Cambridge, MA: MIT Press; 1989. Caplan D, Waters G. Issues arising regarding the nature and consequences of reproduction conduction aphasia. In: Kohn SE, editor. Conduction aphasia. Hillsdale, NJ: Lawrence Erlbaum; 1992. p. 117–49. Wilshire CE, McCarthy RA. Experimental investigations of an impairment in phonological encoding. Cogn Neuropsychol. 1996;13(7):1059–98. Dell GS, Schwartz MF, Martin N, et al. Lexical access in aphasic and nonaphasic speakers. Psychol Rev. 1997;104(4):801–38. • Acheson DJ, Hamidi M, Binder JR, Postle BR. A common neural substrate for language production and verbal working memory. J Cogn Neurosci. 2011;23:1358–67. This study presents combined fMRI and transcranial magnetic stimulation evidence for a common posterior STG localization for phonological representation and phonological short-term memory . Booth JR, Burman DD, Meyer JR, et al. Functional anatomy of intra- and cross-modal lexical tasks. NeuroImage. 2002;16:7–22. Xu B, Grafman J, Gaillard WD, et al. Neuroimaging reveals automatic speech coding during perception of written word meaning. NeuroImage. 2002;17(2):859–70. Hickok G, Buchsbaum B, Humphries C, Muftuler T. Auditory-motor interaction revealed by fMRI: speech, music, and working memory in area Spt. J Cogn Neurosci. 2003;15(5):673–82. Indefrey P, Levelt WJM. The spatial and temporal signatures of word production components. Cognition. 2004;92(1–2):101–44. Buchsbaum BR, Olsen RK, Koch P, Berman KF. Human dorsal and ventral auditory streams subserve rehearsal-based and echoic processes during verbal working memory. Neuron. 2005;48(4):687–97. Burton MW, Locasto PC, Krebs-Noble D, Gullapalli RP. A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing. NeuroImage. 2005;26(3):647–61. Graves WW, Grabowski TJ, Mehta S, Gordon JK. A neural signature of phonological access: distinguishing the effects of word frequency from familiarity and length in overt picture naming. J Cogn Neurosci. 2007;19(4):617–31. Bruno JL, Zumberge A, Manis FR, et al. Sensitivity to orthographic familiarity in the occipito-temporal region. NeuroImage. 2008;39:1988–2001. Wilson SM, Isenberg AK, Hickok G. Neural correlates of word production stages delineated by parametric modulation of psycholinguistic variables. Hum Brain Mapp. 2009;30:3596–608. Wilson LB, Tregellas JR, Slason E, et al. Implicit phonological priming during visual word recognition. NeuroImage. 2011;55(2):724–31. • Pillay SB, Stengel BC, Humphries C, et al. Cerebral localization of impaired phonological retrieval during rhyme judgment. Ann Neurol. 2014;76:738–46. This study presents lesion evidence linking the classical Wernicke's area with pre-articulatory (i.e., silent) retrieval of phonological word forms. Gorno-Tempini ML, Brambati SM, Ginex V, et al. The logopenic/phonological variant of primary progressive aphasia. Neurology. 2008;71(16):1227–34. Rohrer JD, Ridgway GR, Crutch SJ, et al. Progressive logopenic/phonological aphasia: erosion of the language network. NeuroImage. 2010;49:984–93. Leyton CE, Ballard KJ, Piguet O, Hodges JR. Phonologic errors as a clinical marker of the logopenic variant of PPA. Neurology. 2014;82(18):1620–7. Blumstein SE, Baker E, Goodglass H. Phonological factors in auditory comprehension in aphasia. Neuropsychologia. 1977;15:19–30. Blumstein SE, Tartter VC, Nigro G, Statlender S. Acoustic cues for the perception of place of articulation in aphasia. Brain Lang. 1984;22:128–49. Boatman D, Hart J, Lesser RP, et al. Right hemisphere speech perception revealed by amobarbital injection and electrical interference. Neurology. 1998;51(2):458–64. Hickok G, Okada K, Barr W, et al. Bilateral capacity for speech sound processing in auditory comprehension: evidence from Wada procedures. Brain Lang. 2008;107:179–84. Buchman AS, Garron DC, Trost-Cardamone JE, et al. Word deafness: one hundred years later. J Neurol Neurosurg Psychiatry. 1986;49:489–99. Poeppel D. Pure word deafness and the bilateral processing of the speech code. Cogn Sci. 2001;25:679–93. Binder JR, Frost JA, Hammeke TA, et al. Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex. 2000;10:512–28. Liebenthal E, Binder JR, Spitzer SM, et al. Neural substrates of phonemic perception. Cereb Cortex. 2005;15:1621–31. • DeWitt I, Rauschecker JP. Phoneme and word recognition in the auditory ventral stream. Proc Natl Acad Sci U S A. 2012;109:E505–14. This careful meta-analysis of fMRI speech perception studies provides strong evidence that auditory cortex specialized for speech perception lies anterior to the classical Wernicke's area . Scott SK, Blank C, Rosen S, Wise RJS. Identification of a pathway for intelligible speech in the left temporal lobe. Brain. 2000;123:2400–6. Binder JR. Wernicke aphasia: a disorder of central language processing. In: D’Esposito ME, editor. Neurological foundations of cognitive neuroscience. Cambridge, MA: MIT Press; 2002. p. 175–238. Kertesz A, Lau WK, Polk M. The structural determinants of recovery in Wernicke’s aphasia. Brain Lang. 1993;44:153–64. Dronkers NF, Redfern BB, Ludy CA. Lesion localization in chronic Wernicke’s aphasia. Brain Lang. 1995;51:62–5. Damasio H, Tranel D, Grabowski T, et al. Neural systems behind word and concept retrieval. Cognition. 2004;92:179–229. Dronkers NF, Wilkins DP, Van Valin RD, et al. Lesion analysis of the brain areas involved in language comprehension. Cognition. 2004;92:145–77. Thothathiri M, Kimberg DY, Schwartz MF. The neural basis of reversible sentence comprehension: evidence from voxel-based lesion symptom mapping in aphasia. J Cogn Neurosci. 2012;24(1):212–22. Damasio H. Cerebral localization of the aphasias. In: Sarno MT, editor. Acquired aphasia. Orlando: Academic Press; 1981. p. 27–50. Kertesz A, Sheppard A, MacKenzie R. Localization in transcortical sensory aphasia. Arch Neurol. 1982;39:475–8. Alexander MP, Hiltbrunner B, Fischer RS. Distributed anatomy of transcortical sensory aphasia. Arch Neurol. 1989;46:885–92. Rapcsak SZ, Rubens AB. Localization of lesions in transcortical aphasia. In: Kertesz A, editor. Localization and neuroimaging in neuropsychology. San Diego: Academic Press; 1994. p. 297–329. Otsuki M, Soma Y, Koyama A, et al. Transcortical sensory aphasia following left frontal infarction. J Neurol. 1998;245:69–76. Maeshima S, Osawa A, Nakayama Y, Miki J. Transcortical sensory aphasia following infarction in the left frontal lobe. Eur Neurol. 2004;52(2):125–8. Sethi NK, Burke L, Torgovnick J, Arsura E. Transcortical sensory aphasia as a result of left frontal cortical-subcortical infarction. A case report. Eur Neurol. 2007;57(1):52–3. Hodges JR, Patterson K, Oxbury S, Funnell E. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain. 1992;115:1783–806. Rohrer JD, Warren JD, Modat M, et al. Patterns of cortical thinning in the language variants of frontotemporal lobar degeneration. Neurology. 2009;72:1562–9. Rogalski E, Cobia D, Harrison TM, et al. Progression of language decline and cortical atrophy in subtypes of primary progressive aphasia. Neurology. 2011;76:1804–10. Bozeat S, Lambon Ralph MA, Patterson K, et al. Nonverbal semantic impairment in semantic dementia. Neuropsychologia. 2000;38:1207–15. Rogers TT, Garrard P, McClelland JL, et al. Structure and deterioration of semantic memory: a neuropsychological and computational investigation. Psychol Rev. 2004;111(1):205–35. Patterson K, Nestor PJ, Rogers TT. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci. 2007;8:976–87. Binder JR, Desai R, Conant LL, Graves WW. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex. 2009;19:2767–96. Thompson-Schill SL, D’Esposito M, Aguirre GK, Farah MJ. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc Natl Acad Sci U S A. 1997;94:14792–7. Wagner AD, Pare-Blagoev EJ, Clark J, Poldrack RA. Recovering meaning: left prefrontal cortex guides semantic retrieval. Neuron. 2001;31:329–38. Novick JM, Trueswell JC, Thompson-Schill SL. Cognitive control and parsing: reexamining the role of Broca’s area in sentence comprehension. Cognitive, Affective, & Behavioral Neuroscience. 2005;5(3):263–81. Jefferies E, Lambon Ralph MA. Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. Brain. 2006;129:2132–47. Damasio AR. Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition. Cognition. 1989;33:25–62. Simmons WK, Barsalou LW. The similarity-in-topography principle: reconciling theories of conceptual deficits. Cogn Neuropsychol. 2003;20(3):451–86. Meyer K, Damasio A. Convergence and divergence in a neural architecture for recognition and memory. Trends Neurosci. 2009;32(7):376–82. Binder JR, Desai RH. The neurobiology of semantic memory. Trends Cogn Sci. 2011;15(11):527–36. Meteyard L, Rodriguez Cuadrado S, Bahrami B, Vigliocco G. Coming of age: a review of embodiment and the neuroscience of semantics. Cortex. 2012;48:788–804. Fernandino L, Binder JR, Desai RH, et al. Concept representation reflects multimodal abstraction: a framework for embodied semantics. Cereb Cortex. 2016;26:2018–34. •• Turken AU, Dronkers NF. The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses. Frontiers in Systems Neuroscience. 2011;5:Article 1. This paper presents a thorough, multimodal examination of connectivity within a broadly distributed network supporting sentence comprehension, suggesting a special role for the posterior left MTG in this function. Pillay SB, Binder JR, Humphries C, et al. Lesion localization of speech comprehension deficits in chronic aphasia. Neurology. 2017;88(10):970–5.