Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-24T20:59:51.263Z Has data issue: false hasContentIssue false
  • English
  • Français

Spared bottom-up but impaired top-down interactive effects during naturalistic language processing in schizophrenia: evidence from the visual-world paradigm

Published online by Cambridge University Press:  22 August 2018

Hugh Rabagliati Open the ORCID record for Hugh Rabagliati [Opens in a new window] ,
Nathaniel Delaney-Busch ,
Jesse Snedeker  and
Gina Kuperberg
Hugh Rabagliati*
Affiliation:
Department of Psychology, Tufts University, Medford, MA 02155, USA Department of Psychology, Harvard University, Cambridge, MA 01238, USA School of Philosophy, Psychology and Language Sciences, University of Edinburgh, Edinburgh, UK
Nathaniel Delaney-Busch
Affiliation:
Department of Psychology, Tufts University, Medford, MA 02155, USA
Jesse Snedeker
Affiliation:
Department of Psychology, Harvard University, Cambridge, MA 01238, USA
Gina Kuperberg
Affiliation:
Department of Psychology, Tufts University, Medford, MA 02155, USA Department of Psychiatry and the Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
*
Author for correspondence: Hugh Rabagliati, E-mail: hugh.rabagliati@ed.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

People with schizophrenia process language in unusual ways, but the causes of these abnormalities are unclear. In particular, it has proven difficult to empirically disentangle explanations based on impairments in the top-down processing of higher level information from those based on the bottom-up processing of lower level information.

Methods

To distinguish these accounts, we used visual-world eye tracking, a paradigm that measures spoken language processing during real-world interactions. Participants listened to and then acted out syntactically ambiguous spoken instructions (e.g. ‘tickle the frog with the feather’, which could either specify how to tickle a frog, or which frog to tickle). We contrasted how 24 people with schizophrenia and 24 demographically matched controls used two types of lower level information (prosody and lexical representations) and two types of higher level information (pragmatic and discourse-level representations) to resolve the ambiguous meanings of these instructions. Eye tracking allowed us to assess how participants arrived at their interpretation in real time, while recordings of participants’ actions measured how they ultimately interpreted the instructions.

Results

We found a striking dissociation in participants’ eye movements: the two groups were similarly adept at using lower level information to immediately constrain their interpretations of the instructions, but only controls showed evidence of fast top-down use of higher level information. People with schizophrenia, nonetheless, did eventually reach the same interpretations as controls.

Conclusions

These data suggest that language abnormalities in schizophrenia partially result from a failure to use higher level information in a top-down fashion, to constrain the interpretation of language as it unfolds in real time.

Keywords

Eye movementslanguagepredictionschizophreniavisual-world paradigm
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 8 , June 2019 , pp. 1335 - 1345
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, RA, Stephan, KE, Brown, HR, Frith, CD and Friston, KJ (2013) The computational anatomy of psychosis. Frontiers in Psychiatry 4, 47.Google Scholar
Adcock, RA, Dale, C, Fisher, M, Aldebot, S, Genevsky, A, Simpson, GV, Nagarajan, S and Vinogradov, S (2009) When top-down meets bottom-up: auditory training enhances verbal memory in schizophrenia. Schizophrenia Bulletin 35, 1132–1141.Google Scholar
Andreasen, NC (1979 a) Thought, language and communication disorders. I. Clinical assessment, definition of terms, and evaluation of their reliability. Archives of General Psychiatry 36, 1315–1321.Google Scholar
Andreasen, NC (1979 b) Thought, language and communication disorders. II. Diagnostic significance. Archives of General Psychiatry 36, 1325–1330.Google Scholar
Andreasen, NC (1984 a) Scale for the Assessment of Negative Symptoms (SANS). Iowa City: The University of Iowa.Google Scholar
Andreasen, NC (1984 b) Scale for the Assessment of Positive Symptoms (SAPS). Iowa City, IA: The University of Iowa.Google Scholar
Andreasen, NC (1986) Scale for assessment of thought, language and communication (TLC). Schizophrenia Bulletin 12, 473–482.Google Scholar
Bambini, V, Arcara, G, Bechi, M, Buonocore, M, Cavallaro, R and Bosia, M (2016) The communicative impairment as a core feature of schizophrenia: frequency of pragmatic deficit, cognitive substrates, and relation with quality of life. Comprehensive Psychiatry 71, 106–120.Google Scholar
Barch, DM and Smith, E (2008) The cognitive neuroscience of working memory: relevance to CNTRICS and schizophrenia. Biological Psychiatry 64, 11–17.Google Scholar
Bates, DM, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Blair, JR and Spreen, O (1989) Predicting premorbid IQ: a revision of the National Adult Reading Test. Clinical Neuropsychologist 3, 129–136.Google Scholar
Bleuler, E (1911/1950) Dementia Praecox, or the Group of Schizophrenias (J. Zinker, Trans.). New York: International Universities Press.Google Scholar
Boudewyn, MA, Carter, CS and Swaab, TY (2012) Cognitive control and discourse comprehension in schizophrenia. Schizophrenia Research and Treatment 2012, 484–502.Google Scholar
Bowie, CR and Harvey, PD (2008) Communication abnormalities predict functional outcomes in chronic schizophrenia: differential associations with social and adaptive functions. Schizophrenia Research 103, 240–247.Google Scholar
Brown, M and Kuperberg, GR (2015) A hierarchical generative framework of language processing: linking language perception, interpretation, and production abnormalities in schizophrenia. Frontiers in Human Neuroscience 9, 643.Google Scholar
Chapman, LJ and Chapman, JP (1973) Problems in the measurement of cognitive deficit. Psychological Bulletin 79, 380–385.Google Scholar
Cienfuegos, A, March, L, Shelley, A-M and Javitt, DC (1999) Impaired categorical perception of synthetic speech sounds in schizophrenia. Biological Psychiatry 45, 82–88.Google Scholar
Cohen, JD and Servan-Schreiber, D (1992) Context, cortex, and dopamine: a connectionist approach to behaviour and biology in schizophrenia. Psychological Review 99, 45–77.Google Scholar
Colle, L, Angeleri, R, Vallana, M, Sacco, K, Bara, BG and Bosco, FM (2013) Understanding the communicative impairments in schizophrenia: a preliminary study. Journal of Communication Disorders 46, 294–308.Google Scholar
Corlett, PR, Frith, CD and Fletcher, PC (2009) From drugs to deprivation: a Bayesian framework for understanding models of psychosis. Psychopharmacology 206, 515–530.Google Scholar
Corlett, PR, Taylor, JR, Wang, XJ, Fletcher, PC and Krystal, JH (2010) Toward a neurobiology of delusions. Progress in Neurobiology 92, 345–369.Google Scholar
Dahan, D and Tanenhaus, MK (2004) Continuous mapping from sound to meaning in spoken-language comprehension: immediate effects of verb-based thematic constraints. Journal of Experimental Psychology: Learning, Memory, and Cognition 30, 498–513.Google Scholar
Dell, GS and Chang, F (2014) The P-chain: relating sentence production and its disorders to comprehension and acquisition. Philosophical Transactions of the Royal Society B: Biological Sciences 369, 20120394.Google Scholar
de Ruiter, JP, Mitterer, H and Enfield, NJ (2006) Projecting the end of a speaker's turn: a cognitive cornerstone of conversation. Language 82, 515–535.Google Scholar
Diehl, JJ, Friedberg, C, Paul, R and Snedeker, J (2015) The use of prosody during syntactic processing in children and adolescents with autism spectrum disorders. Development and Psychopathology 27, 867–884.Google Scholar
Ditman, T and Kuperberg, GR (2007) The time course of building discourse coherence in schizophrenia: an ERP investigation. Psychophysiology 44, 991–1001.Google Scholar
Ditman, T, Goff, D and Kuperberg, GR (2011) Slow and steady: sustained effects of lexico-semantic associations can mediate referential impairments in schizophrenia. Cognitive, Affective, & Behavioral Neuroscience 11, 245–258.Google Scholar
Elman, JL, Hare, M and McRae, K (2004) Cues, constraints, and competition in sentence processing. In Beyond Nature-Nurture: Essays in Honor of Elizabeth Bates. Mahwah, NJ: Lawrence Erlbaum Associates Publishers, pp. 111–138.Google Scholar
Elvevåg, B, Foltz, PW, Weinberger, DR and Goldberg, TE (2007) Quantifying incoherence in speech: an automated methodology and novel application to schizophrenia. Schizophrenia Research 93, 304–316.Google Scholar
First, M, Spitzer, R, Miriam, G and Williams, J (2002 a) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition (SCID-I/NP). Retrieved from New York.Google Scholar
First, M, Spitzer, R, Miriam, G and Williams, J (2002 b) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCID-I/P). Retrieved from New York.Google Scholar
Fletcher, PC and Frith, CD (2009) Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nature Reviews Neuroscience 10, 48–58.Google Scholar
Ford, JM and Mathalon, DH (2012) Anticipating the future: automatic prediction failures in schizophrenia. International Journal of Psychophysiology 83, 232–239.Google Scholar
Frith, CD (2004) Schizophrenia and theory of mind. Psychological Medicine 34, 385–389.Google Scholar
Gambi, C, Pickering, MJ and Rabagliati, H (2016) Beyond associations: sensitivity to structure in pre-schoolers’ linguistic predictions. Cognition 157, 340–351.Google Scholar
Gardner, DM, Murphy, AL, O'Donnell, H, Centorrino, F and Baldessarini, RJ (2010) International consensus study of antipsychotic dosing. American Journal of Psychiatry 167, 686–693.Google Scholar
Gold, JM and Dickinson, D (2012) ‘Generalized cognitive deficit’ in schizophrenia: overused or underappreciated? Schizophrenia Bulletin 39, 263–265.Google Scholar
Harrow, M, Lanin-Kettering, I and Miller, JG (1989) Impaired perspective and thought pathology in schizophrenic and psychotic disorders. Schizophrenia Bulletin 15, 605–623.Google Scholar
Hemsley, DR (1993) A simple (or simplistic?) cognitive model for schizophrenia. Behaviour Research and Therapy 31, 633–645.Google Scholar
Hollingshead, AB (1965) Two Factor Index of Social Position. New Haven, CT: Yale University Press.Google Scholar
Holshausen, K, Harvey, PD, Elvevåg, B, Foltz, PW and Bowie, CR (2014) Latent semantic variables are associated with formal thought disorder and adaptive behavior in older inpatients with schizophrenia. Cortex 55, 88–96.Google Scholar
Huang, YT and Snedeker, J (2009 a) Online interpretation of scalar quantifiers: insight into the semantics-pragmatics interface. Cognitive Psychology 58, 376–415.Google Scholar
Huang, YT and Snedeker, J (2009 b) Semantic meaning and pragmatic interpretation in 5-year-olds: evidence from real-time spoken language comprehension. Developmental Psychology 45, 1723–1739.Google Scholar
Huang, YT, Stranahan, L and Snedeker, J (2017) Reconsideration on linking eye-movement data with argument realization. Paper presented at the 39th Annual Meeting of the Cognitive Science Society, London, UK.Google Scholar
Iacono, WG (1981) Dissociation of smooth-pursuit and saccadic eye tracking in remitted schizophrenics. Archives of General Psychiatry 38, 991.Google Scholar
Jahshan, C, Wynn, JK and Green, MF (2013) Relationship between auditory processing and affective prosody in schizophrenia. Schizophrenia Research 143, 348–353.Google Scholar
Javitt, DC (2009) When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. Annual Review of Clinical Psychology 5, 249–275.Google Scholar
Javitt, DC and Freedman, R (2015) Sensory processing dysfunction in the personal experience and neuronal machinery of schizophrenia. American Journal of Psychiatry 172, 17–31.Google Scholar
Kantrowitz, JT, Hoptman, MJ, Leitman, DI, Silipo, G and Javitt, DC (2014) The 5% difference: early sensory processing predicts sarcasm perception in schizophrenia and schizo-affective disorder. Psychological Medicine 44, 25–36.Google Scholar
Kasai, K, Nakagome, K, Itoh, K, Koshida, I, Hata, A, Iwanami, A, Fukuda, M and Kato, N (2002) Impaired cortical network for preattentive detection of change in speech sounds in schizophrenia: a high-resolution event-related potential study. American Journal of Psychiatry 159, 546–553.Google Scholar
Keysar, B, Barr, DJ, Balin, JA and Brauner, JS (2000) Taking perspective in conversation: the role of mutual knowledge in comprehension. Psychological Science 11, 32–38.Google Scholar
Kim, H, Somerville, LH, Johnstone, T, Polis, S, Alexander, AL, Shin, LM and Whalen, PJ (2004) Contextual modulation of amygdala responsivity to surprised faces. Journal of Cognitive Neuroscience 16, 1730–1745.Google Scholar
Kleinschmidt, DF and Jaeger, FT (2015) Robust speech perception: recognize the familiar, generalize to the similar, and adapt to the novel. Psychological Review 122, 148–203.Google Scholar
Kreher, DA, Goff, D and Kuperberg, GR (2009) Why all the confusion? Experimental task explains discrepant semantic priming effects in schizophrenia under ‘automatic’ conditions: evidence from event-related potentials. Schizophrenia Research 111, 174–181.Google Scholar
Kuperberg, GR (2010 a) Language in schizophrenia part 1: an introduction. Language and Linguistics Compass 4, 576–589.Google Scholar
Kuperberg, GR (2010 b) Language in schizophrenia Part 2: what can psycholinguistics bring to the study of schizophrenia…and vice versa? Language and Linguistics Compass 4, 590–604.Google Scholar
Kuperberg, GR and Jaeger, TF (2016) What do we mean by prediction in language comprehension? Language, Cognition, and Neuroscience 31, 32–59.Google Scholar
Kuperberg, GR, McGuire, PK and David, A (1998) Reduced sensitivity to linguistic context in schizophrenic thought disorder: evidence from online monitoring for words in linguistically-anomalous sentences. Journal of Abnormal Psychology 107, 423–434.Google Scholar
Kuperberg, GR, Sitnikova, T, Goff, D and Holcomb, PJ (2006) Making sense of sentences in schizophrenia: electrophysiological evidence for abnormal interactions between semantic and syntactic processing. Journal of Abnormal Psychology 115, 251–265.Google Scholar
Kuperberg, GR, Ditman, T and Choi Perrachione, A (2018) When proactivity fails: an electrophysiological study of establishing reference in schizophrenia. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging 3, 77–87.Google Scholar
Leitman, DI, Foxe, JJ, Butler, PD, Saperstein, A, Revheim, N and Javitt, DC (2005) Sensory contributions to impaired prosodic processing in schizophrenia. Biological Psychiatry 58, 56–61.Google Scholar
Magyari, L and de Ruiter, JP (2012) Prediction of turn-ends based on anticipation of upcoming words. Frontiers in Psychology 3, 376.Google Scholar
Mathalon, DH, Faustman, WO and Ford, JM (2002) N400 and automatic semantic processing abnormalities in patients with schizophrenia. Archives of General Psychiatry 59, 641–648.Google Scholar
McCabe, R, Leudar, I and Antaki, C (2004) Do people with schizophrenia display theory of mind deficits in clinical interactions? Psychological Medicine 34, 401–412.Google Scholar
McClelland, JL and Rumelhart, DE (1981) An interactive activation model of context effects in letter perception: I. An account of basic findings. Psychological Review 88, 375–407.Google Scholar
Meilijson, SR, Kasher, A and Elizur, A (2004) Language performance in chronic schizophrenia. Journal of Speech Language and Hearing Research 47, 695.Google Scholar
Minzenberg, MJ, Ober, BA and Vinogradov, S (2002) Semantic priming in schizophrenia: a review and synthesis. Journal of the International Neuropsychological Society 8, 699–720.Google Scholar
Mirman, D, Dixon, JA and Magnuson, JS (2008) Statistical and computational models of the visual world paradigm: growth curves and individual differences. Journal of Memory and Language 59, 475–494.Google Scholar
Pawełczyk, A, Kotlicka-Antczak, M, Łojek, E, Ruszpel, A and Pawełczyk, T (2017) Schizophrenia patients have higher-order language and extralinguistic impairments. Schizophrenia Research 192, 274–280.Google Scholar
Rabagliati, H, Gambi, C and Pickering, MJ (2014) Learning to predict or predicting to learn? Language, Cognition and Neuroscience 31, 94–105.Google Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.Google Scholar
Rescorla, RA (1988) Pavlovian conditioning: it's not what you think it is. American Psychologist 43, 151.Google Scholar
Revheim, ME, Hole, KH, Bruland, OS, Reitan, E, Bjerkehagen, B, Julsrud, L and Seierstad, T (2014) Multimodal functional imaging for early response assessment in GIST patients treated with imatinib. Acta Oncologica 53, 143–148.Google Scholar
Rumelhart, DE and McClelland, JL (1982) An interactive activation model of context effects in letter perception: II. The contextual enhancement effect and some tests and extensions of the model. Psychological Review 89, 60–94.Google Scholar
Sedivy, JC, Tanenhaus, MK, Chambers, CG and Carlson, GN (1999) Achieving incremental semantic interpretation through contextual representation. Cognition 71, 109–147.Google Scholar
Silverstein, S, Hatashita-Wong, M, Schenkel, L, Wilkniss, S, Kovács, I, Fehér, A, Smith, T, Goicochea, C, Uhlhaas, P, Carpiniello, K and Savitz, A (2006) Reduced top-down influences in contour detection in schizophrenia. Cognitive Neuropsychiatry 11, 112–132.Google Scholar
Silverstein, SM, Matteson, S and Knight, RA (1996) Reduced top-down influence in auditory perceptual organization in schizophrenia. Journal of Abnormal Psychology 105, 663–667.Google Scholar
Sitnikova, T, Salisbury, DF, Kuperberg, GR and Holcomb, PJ (2002) Electrophysiological insights into language processing in schizophrenia. Psychophysiology 39, 851–860.Google Scholar
Snedeker, J and Trueswell, JC (2004) The developing constraints on parsing decisions: the role of lexical-biases and referential scenes in child and adult sentence processing. Cognitive Psychology 49, 238–299.Google Scholar
Snedeker, J and Yuan, S (2008) Effects of prosodic and lexical constraints on parsing in young children (and adults). Journal of Memory and Language 58, 574–608.Google Scholar
Spitzer, M, Braun, U, Hermle, L and Maier, S (1993) Associative semantic network dysfunction in thought-disordered schizophrenic patients: direct evidence from indirect semantic priming. Biological Psychiatry 34, 864–877.Google Scholar
Swaab, TY, Boudewyn, MA, Long, DL, Luck, SJ, Kring, AM, Ragland, JD, Ranganath, C, Lesh, T, Niendam, T, Solomon, M and Mangun, GR (2013) Spared and impaired spoken discourse processing in schizophrenia: effects of local and global language context. Journal of Neuroscience 33, 15578–15587.Google Scholar
Tanenhaus, MK and Trueswell, JC (2006) Eye movements and spoken language comprehension. In Traxler, MJ and Gernsbacher, MA (eds), Handbook of Psycholinguistics, 2nd Edn. Oxford: Oxford University Press, pp. 863–900.Google Scholar
Tanenhaus, MK, Spivey-Knowlton, MJ, Eberhard, KM and Sedivy, JC (1995) Integration of visual and linguistic information in spoken language comprehension. Science 268, 1632–1634.Google Scholar
Titone, D and Levy, DL (2004) Lexical competition and spoken word identification in schizophrenia. Schizophrenia Research 68, 75–85.Google Scholar
Titone, D, Levy, DL and Holzman, PS (2000) Contextual insensitivity in schizophrenic language processing: evidence from lexical ambiguity. Journal of Abnormal Psychology 109, 761–767.Google Scholar
Trueswell, JC, Sekerina, I, Hill, NM and Logrip, ML (1999) The kindergarten-path effect: studying on-line sentence processing in young children. Cognition 73, 89–134.Google Scholar
Whitford, V, O'Driscoll, GA, Pack, CC, Joober, R, Malla, A and Titone, D (2013) Reading impairments in schizophrenia relate to individual differences in phonological processing and oculomotor control: evidence from a gaze-contingent moving window paradigm. Journal of Experimental Psychology: General 142, 57–75.Google Scholar
Whitford, V, O'Driscoll, GA and Titone, D (2017) Reading deficits in schizophrenia and their relationship to developmental dyslexia: a review. Schizophrenia Research 193, 11–22.Google Scholar
Supplementary material: File

Rabagliati et al. supplementary material

Rabagliati et al. supplementary material 1

Download Rabagliati et al. supplementary material(File)
File 1.1 MB