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Brain substrates of perceived spatial separation between speech sources under simulated reverberant listening conditions in schizophrenia

Published online by Cambridge University Press:  01 October 2015

Y. Zheng
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
C. Wu
Affiliation:
Department of Psychology, School of Life Sciences, McGovern Institute for Brain Research at PKU, Key Laboratory on Machine Perception (Ministry of Education), Peking University, Beijing 100871, People's Republic of China
J. Li
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
H. Wu
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
S. She
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
S. Liu
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
H. Wu
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
L. Mao
Affiliation:
Department of Psychology, School of Life Sciences, McGovern Institute for Brain Research at PKU, Key Laboratory on Machine Perception (Ministry of Education), Peking University, Beijing 100871, People's Republic of China
Y. Ning
Affiliation:
Guangzhou Brain Hospital, the Affiliated Hospital of Guangzhou Medical University, Guangzhou 510370, People's Republic of China
L. Li*
Affiliation:
Department of Psychology, School of Life Sciences, McGovern Institute for Brain Research at PKU, Key Laboratory on Machine Perception (Ministry of Education), Peking University, Beijing 100871, People's Republic of China Beijing Institute for Brain Disorders, Capital Medical University, Beijing, People's Republic of China
*
*Address for correspondence: L. Li, Ph.D., Department of Psychology, Peking University, 5 Yiheyuan Road, Beijing 100871, People's Republic of China. (Email: liangli@pku.edu.cn)

Abstract

Background

People with schizophrenia recognize speech poorly under multiple-people-talking (informational masking) conditions. In reverberant environments, direct-wave signals from a speech source are perceptually integrated with the source reflections (the precedence effect), forming perceived spatial separation (PSS) between different sources and consequently improving target-speech recognition against informational masking. However, the brain substrates underlying the schizophrenia-related vulnerability to informational masking and whether schizophrenia affects the unmasking effect of PSS are largely unknown.

Method

Using psychoacoustic testing and functional magnetic resonance imaging, respectively, the speech recognition under either the PSS or perceived spatial co-location (PSC) condition and the underlying brain substrates were examined in 20 patients with schizophrenia and 16 healthy controls.

Results

Speech recognition was worse in patients than controls. Under the PSS (but not PSC) condition, speech recognition was correlated with activation of the superior parietal lobule (SPL), and target speech-induced activation of the SPL, precuneus, middle cingulate cortex and caudate significantly declined in patients. Moreover, the separation (PSS)-against-co-location (PSC) contrast revealed (1) activation of the SPL, precuneus and anterior cingulate cortex in controls, (2) suppression of the SPL and precuneus in patients, (3) activation of the pars triangularis of the inferior frontal gyrus and middle frontal gyrus in both controls and patients, (4) activation of the medial superior frontal gyrus in patients, and (5) impaired functional connectivity of the SPL in patients.

Conclusions

Introducing the PSS listening condition efficiently reveals both the brain substrates underlying schizophrenia-related speech-recognition deficits against informational masking and the schizophrenia-related neural compensatory strategy for impaired SPL functions.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2015 

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References

Ali, N, Green, DW, Kherif, F, Devlin, JT, Price, CJ (2010). The role of the left head of caudate in suppressing irrelevant words. Journal of Cognitive Neuroscience 22, 23692386.CrossRefGoogle ScholarPubMed
Andrews-Hanna, JR (2012). The brain's default network and its adaptive role in internal mentation. Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry 18, 251270.Google Scholar
Andrews-Hanna, JR, Smallwood, J, Spreng, RN (2014). The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Annals of the New York Academy of Sciences 1316, 2952.CrossRefGoogle ScholarPubMed
Apps, MAJ, Lockwood, PL, Balsters, JH (2013). The role of the midcingulate cortex in monitoring others’ decisions. Frontiers in Neuroscience 7, 251.Google Scholar
Brungart, DS, Simpson, BD, Freyman, RL (2005). Precedence-based speech segregation in a virtual auditory environment. Journal of the Acoustical Society of America 118, 32413251.Google Scholar
Carreiras, M, Mechelli, A, Estévez, A, Price, CJ (2007). Brain activation for lexical decision and reading aloud: two sides of the same coin? Journal of Cognitive Neuroscience 19, 433444.CrossRefGoogle ScholarPubMed
Cavanna, AE, Trimble, MR (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564583.Google Scholar
Culling, JF, Hodder, KI, Toh, CY (2003). Effects of reverberation on perceptual segregation of competing voices. Journal of the Acoustical Society of America 114, 28712876.Google Scholar
Darwin, CJ, Hukin, RW (2000). Effects of reverberation on spatial, prosodic, and vocal-tract size cues to selective attention. Journal of the Acoustical Society of America 108, 335342.Google Scholar
Ding, N, Simon, JZ (2012). Emergence of neural encoding of auditory objects while listening to competing speakers. Proceedings of the National Academy of Sciences of the United States of America 109, 1185411859.CrossRefGoogle ScholarPubMed
Dosenbach, NU, Fair, DA, Miezin, FM, Cohen, AL, Wenger, KK, Dosenbach, RA, Fox, MD, Snyder, AZ, Vincent, JL, Raichle, ME (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences of the United States of America 104, 1107311078.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JB (2012). Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I), Clinician Version. Administration Booklet. American Psychiatric Press, Inc.: Washington, DC.Google Scholar
Fish, SC, Granholm, E (2008). Easier tasks can have higher processing loads: task difficulty and cognitive resource limitations in schizophrenia. Journal of Abnormal Psychology 117, 355363.Google Scholar
Fornito, A, Yoon, J, Zalesky, A, Bullmore, ET, Carter, CS (2011). General and specific functional connectivity disturbances in first-episode schizophrenia during cognitive control performance. Biological Psychiatry 70, 6472.CrossRefGoogle ScholarPubMed
Freyman, RL, Clifton, RK, Litovsky, RY (1991). Dynamic processes in the precedence effect. Journal of the Acoustical Society of America 90, 874884.CrossRefGoogle ScholarPubMed
Freyman, RL, Helfer, KS, McCall, DD, Clifton, RK (1999). The role of perceived spatial separation in the unmasking of speech. Journal of the Acoustical Society of America 106, 35783588.Google Scholar
Friston, KJ, Buechel, C, Fink, GR, Morris, J, Rolls, E, Dolan, RJ (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6, 218229.Google Scholar
Friston, KJ, Williams, S, Howard, R, Frackowiak, RS, Turner, R (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine 35, 346355.Google Scholar
Gao, B, Wang, Y, Liu, W, Chen, Z, Zhou, H, Yang, J, Cohen, Z, Zhu, Y, Zang, Y (2015). Spontaneous activity associated with delusions of schizophrenia in the left medial superior frontal gyrus: a resting-state fMRI study. PLOS ONE 10, e0133766.Google ScholarPubMed
Gjerde, PF (1983). Attentional capacity dysfunction and arousal in schizophrenia. Psychological Bulletin 93, 5772.Google Scholar
Hall, DA, Haggard, MP, Akeroyd, MA, Palmer, AR, Summerfield, AQ, Elliott, MR, Gurney, EM, Bowtell, RW (1999). Sparse temporal sampling in auditory fMRI. Human Brain Mapping 7, 213223.Google Scholar
Helfer, KS (1997). Auditory and auditory-visual perception of clear and conversational speech. Journal of Speech, Language, and Hearing Research 40, 432443.Google Scholar
Hill, KT, Miller, LM (2010). Auditory attentional control and selection during cocktail party listening. Cerebral Cortex 20, 583590.Google Scholar
Huang, Y, Huang, Q, Chen, X, Qu, T, Wu, X, Li, L (2008). Perceptual integration between target speech and target-speech reflection reduces masking for target-speech recognition in younger adults and older adults. Hearing Research 244, 5165.CrossRefGoogle ScholarPubMed
Huang, Y, Li, J, Zou, X, Qu, T, Wu, X, Mao, L, Wu, Y, Li, L (2011). Perceptual fusion tendency of speech sounds. Journal of Cognitive Neuroscience 23, 10031014.Google Scholar
Jeurissen, D, Sack, AT, Roebroeck, A, Russ, BE, Pascual-Leone, A (2014). TMS affects moral judgment, showing the role of DLPFC and TPJ in cognitive and emotional processing. Frontiers in Neuroscience 8, 18.Google Scholar
Ketteler, D, Kastrau, F, Vohn, R, Huber, W (2008). The subcortical role of language processing. High level linguistic features such as ambiguity-resolution and the human brain; an fMRI study. NeuroImage 39, 20022009.Google Scholar
Kidd, G, Mason, CR, Brughera, A, Hartmann, WM (2005). The role of reverberation in release from masking due to spatial separation of sources for speech identification. Acta Acustica United with Acustica 91, 526536.Google Scholar
Koehnke, J, Besing, JM (1996). A procedure for testing speech intelligibility in a virtual listening environment. Ear and Hearing 17, 211217.Google Scholar
Krueger, F, Fischer, R, Heinecke, A, Hagendorf, H (2007). An fMRI investigation into the neural mechanisms of spatial attentional selection in a location-based negative priming task. Brain Research 1174, 110119.Google Scholar
Lesh, TA, Niendam, TA, Minzenberg, MJ, Carter, CS (2011). Cognitive control deficits in schizophrenia: mechanisms and meaning. Neuropsychopharmacology 36, 316338.Google Scholar
Li, CSR, Yan, P, Sinha, R, Lee, TW (2008). Subcortical processes of motor response inhibition during a stop signal task. NeuroImage 41, 13521363.Google Scholar
Li, H, Kong, L, Wu, X, Li, L (2013). Primitive auditory memory is correlated with spatial unmasking that is based on direct-reflection integration. PLOS ONE 8, e63106.Google ScholarPubMed
Li, L, Daneman, M, Qi, JG, Schneider, BA (2004). Does the information content of an irrelevant source differentially affect spoken word recognition in younger and older adults? Journal of Experimental Psychology: Human Perception and Performance 30, 10771091.Google ScholarPubMed
Li, L, Qi, JG, He, Y, Alain, C, Schneider, BA (2005). Attribute capture in the precedence effect for long-duration noise sounds. Hearing Research 202, 235247.Google Scholar
Liu, L, Peng, D, Ding, G, Jin, Z, Zhang, L, Li, K, Chen, C (2006). Dissociation in the neural basis underlying Chinese tone and vowel production. NeuroImage 29, 515523.Google Scholar
Mazoyer, P, Wicker, B, Fonlupt, P (2002). A neural network elicited by parametric manipulation of the attention load. Neuroreport 13, 23312334.Google Scholar
McGettigan, C, Faulkner, A, Altarelli, I, Obleser, J, Baverstock, H, Scott, SK (2012). Speech comprehension aided by multiple modalities: behavioural and neural interactions. Neuropsychologia 50, 762776.Google Scholar
Menon, V, Adleman, NE, White, CD, Glover, GH, Reiss, AL (2001). Error-related brain activation during a go/nogo response inhibition task. Human Brain Mapping 12, 131143.Google Scholar
Mickey, BJ, Dalack, GW (2005). Auditory gating in schizophrenia: a pilot study of the precedence effect. Schizophrenia Research 73, 327331.Google Scholar
Nuechterlein, KH, Dawson, ME (1984). Information processing and attentional functioning in the developmental course of schizophrenic disorders. Schizophrenia Bulletin 10, 160203.Google Scholar
Nuechterlein, KH, Dawson, ME, Green, MF (1994). Information-processing abnormalities as neuropsychological vulnerability indicators for schizophrenia. Acta Psychiatrica Scandinavica 90, 7179.CrossRefGoogle Scholar
Pollmann, S, Weidner, R, Humphreys, GW, Olivers, CN, Müller, K, Lohmann, G, Wiggins, CJ, Watson, DG (2003). Separating distractor rejection and target detection in posterior parietal cortex – an event-related fMRI study of visual marking. NeuroImage 18, 310323.Google Scholar
Qu, T, Xiao, Z, Gong, M, Huang, Y, Li, X, Wu, X (2008). Distance dependent head-related transfer function database of KEMAR. In IEEE International Conference on Audio, Language and Image Processing, 2008, pp. 466470. IEEE. http://www.ieee.org/conferences_events/conferences/conferencedetails/index.html?Conf_ID=13439.Google Scholar
Qu, T, Xiao, Z, Gong, M, Huang, Y, Li, X, Wu, X (2009). Distance-dependent head-related transfer functions measured with high spatial resolution using a spark gap. IEEE Transactions on Audio, Speech, and Language Processing 17, 11241132.Google Scholar
Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America 98, 676682.Google Scholar
Rakerd, B, Aaronson, NL, Hartmann, WM (2006). Release from speech-on-speech masking by adding a delayed masker at a different location. Journal of the Acoustical Society of America 119, 15971605.Google Scholar
Renier, LA, Anurova, I, De Volder, AG, Carlson, S, VanMeter, J, Rauschecker, JP (2009). Multisensory integration of sounds and vibrotactile stimuli in processing streams for “what” and “where”. Journal of Neuroscience 29, 1095010960.CrossRefGoogle Scholar
Repovs, G, Csernansky, JG, Barch, DM (2011). Brain network connectivity in individuals with schizophrenia and their siblings. Biological Psychiatry 69, 967973.Google Scholar
Rushworth, M, Walton, ME, Kennerley, SW, Bannerman, DM (2004). Action sets and decisions in the medial frontal cortex. Trends in Cognitive Sciences 8, 410417.Google Scholar
Schmidt, A, Smieskova, R, Aston, J, Simon, A, Allen, P, Fusar-Poli, P, McGuire, PK, Riecher-Rössler, A, Stephan, KE, Borgwardt, S (2013). Brain connectivity abnormalities predating the onset of psychosis: correlation with the effect of medication. JAMA Psychiatry 70, 903912.Google Scholar
Schmidt, A, Smieskova, R, Simon, A, Allen, P, Fusar-Poli, P, McGuire, PK, Bendfeldt, K, Aston, J, Lang, UE, Walter, M, Radue, EW, Rössler, AR, Borgwardt, SJ (2014). Abnormal effective connectivity and psychopathological symptoms in the psychosis high-risk state. Journal of Psychiatry and Neuroscience 39, 239248.CrossRefGoogle ScholarPubMed
Schulz, KP, Bédard, A-CV, Czarnecki, R, Fan, J (2011). Preparatory activity and connectivity in dorsal anterior cingulate cortex for cognitive control. NeuroImage 57, 242250.Google Scholar
Schumacher, EH, Elston, PA, D'Esposito, M (2003). Neural evidence for representation-specific response selection. Journal of Cognitive Neuroscience 15, 11111121.Google Scholar
Scott, SK, McGettigan, C (2013). The neural processing of masked speech. Hearing Research 303, 5866.Google Scholar
Scott, SK, Rosen, S, Wickham, L, Wise, RJ (2004). A positron emission tomography study of the neural basis of informational and energetic masking effects in speech perception. Journal of the Acoustical Society of America 115, 813821.Google Scholar
Scott, SK, Wise, RJS (2003). PET and fMRI studies of the neural basis of speech perception. Speech Communication 41, 2334.Google Scholar
Seidman, LJ, Van Manen, K, Turner, WM, Gamser, DM, Faraone, SV, Goldstein, JM, Tsuang, MT (1998). The effects of increasing resource demand on vigilance performance in adults with schizophrenia or developmental attentional/learning disorders: a preliminary study. Schizophrenia Research 34, 101112.Google Scholar
Serences, JT, Yantis, S (2007). Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex. Cerebral Cortex 17, 284293.Google Scholar
Shackman, AJ, Salomons, TV, Slagter, HA, Fox, AS, Winter, JJ, Davidson, RJ (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Review Neuroscience 12, 154167.Google Scholar
Shenhav, A, Botvinick, MM, Cohen, JD (2013). The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 79, 217240.Google Scholar
Shomstein, S, Yantis, S (2006). Parietal cortex mediates voluntary control of spatial and nonspatial auditory attention. Journal of Neuroscience 26, 435439.CrossRefGoogle ScholarPubMed
Si, TM, Yang, JZ, Shu, L, Wang, XL, Kong, QM, Zhou, M, Li, XN (2004). The reliability, validity of PANSS (Chinese version), and its implication. Chinese Mental Health Journal 18, 4547.Google Scholar
Sokol-Hessner, P, Hutcherson, C, Hare, T, Rangel, A (2012). Decision value computation in DLPFC and VMPFC adjusts to the available decision time. European Journal of Neuroscience 35, 10651074.Google Scholar
Tan, H, Callicott, JH, Weinberger, DR (2007). Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cerebral Cortex 17, i171i181.Google Scholar
Verleger, R, Talamo, S, Simmer, J, Śmigasiewicz, K, Lencer, R (2013). Neurophysiological sensitivity to attentional overload in patients with psychotic disorders. Clinical Neurophysiology 124, 881892.Google Scholar
Vickery, TJ, Jiang, YV (2009). Inferior parietal lobule supports decision making under uncertainty in humans. Cerebral Cortex 19, 916925.Google Scholar
Vouloumanos, A, Kiehl, K, Werker, J, Liddle, P (2001). Detection of sounds in the auditory stream: event-related fMRI evidence for differential activation to speech and nonspeech. Journal of Cognitive Neuroscience 13, 9941005.Google Scholar
Wallach, H, Newman, EB, Rosenzweig, MR (1949). The precedence effect in sound localization. American Journal of Psychology 62, 315336.Google Scholar
Whitfield-Gabrieli, S, Thermenos, HW, Milanovic, S, Tsuang, MT, Faraone, SV, McCarley, RW, Shenton, ME, Green, AI, Nieto-Castanon, A, LaViolette, P, Wojcik, J, Gabrieli, JD, Seidman, LJ (2009). Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 106, 12791284.Google Scholar
Wild, CJ, Davis, MH, Johnsrude, IS (2012). Human auditory cortex is sensitive to the perceived clarity of speech. NeuroImage 60, 14901502.Google Scholar
Wojciulik, E, Kanwisher, N (1999). The generality of parietal involvement in visual attention. Neuron 23, 747764.Google Scholar
Wu, C, Cao, S, Wu, X, Li, L (2013). Temporally pre-presented lipreading cues release speech from informational masking. Journal of the Acoustical Society of America 133, L281L285.Google Scholar
Wu, C, Cao, S, Zhou, F, Wang, C, Wu, X, Li, L (2012). Masking of speech in people with first-episode schizophrenia and people with chronic schizophrenia. Schizophrenia Research 134, 3341.Google Scholar
Wu, X, Wang, C, Chen, J, Qu, H, Li, W, Wu, Y, Schneider, BA, Li, L (2005). The effect of perceived spatial separation on informational masking of Chinese speech. Hearing Research 199, 110.Google Scholar
Wu, ZM, Chen, ML, Wu, XH, Li, L (2014). Interaction between auditory and motor systems in speech perception. Neuroscience Bulletin 30, 490496.Google Scholar
Yang, Z, Chen, J, Huang, Q, Wu, X, Wu, Y, Schneider, BA, Li, L (2007). The effect of voice cuing on releasing Chinese speech from informational masking. Speech Communication 49, 892904.Google Scholar
Yantis, S, Schwarzbach, J, Serences, JT, Carlson, RL, Steinmetz, MA, Pekar, JJ, Courtney, SM (2002). Transient neural activity in human parietal cortex during spatial attention shifts. Nature Neuroscience 5, 9951002.Google Scholar
Yu, Q, Allen, EA, Sui, J, Arbabshirani, MR, Pearlson, G, Calhoun, VD (2012). Brain connectivity networks in schizophrenia underlying resting state functional magnetic resonance imaging. Current Topics in Medicinal Chemistry 12, 24152425.Google Scholar
Zhang, S, Li, C-SR (2012). Functional connectivity mapping of the human precuneus by resting state fMRI. NeuroImage 59, 35483562.Google Scholar
Zündorf, IC, Lewald, J, Karnath, H (2013). Neural correlates of sound localization in complex acoustic environments. PLOS ONE 8, e64259.Google Scholar
Zurek, PM (1980). The precedence effect and its possible role in the avoidance of interaural ambiguities. Journal of the Acoustical Society of America 67, 952964.Google Scholar
Zurek, PM, Freyman, RL, Balakrishnan, U (2004). Auditory target detection in reverberation. Journal of the Acoustical Society of America 115, 16091620.Google Scholar
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