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Antisaccade error rates and gap effects in psychosis syndromes from bipolar-schizophrenia network for intermediate phenotypes 2 (B-SNIP2)

Published online by Cambridge University Press:  24 February 2021

Ling-Yu Huang
Affiliation:
Departments of Psychology & Neuroscience, University of Georgia, Athens, GA, USA
Brooke S. Jackson
Affiliation:
Departments of Psychology & Neuroscience, University of Georgia, Athens, GA, USA
Amanda L. Rodrigue
Affiliation:
Department of Psychiatry, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA
Carol A. Tamminga
Affiliation:
Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, USA
Elliot S. Gershon
Affiliation:
Department of Psychiatry and Behavioral Neuroscience, University of Chicago, Chicago, IL, USA
Godfrey D. Pearlson
Affiliation:
The Institute of Living, Hartford, CT, USA
Matcheri S. Keshavan
Affiliation:
Department of Psychiatry, Harvard Medical School, Boston, MA, USA
Sarah S. Keedy
Affiliation:
Department of Psychiatry and Behavioral Neuroscience, University of Chicago, Chicago, IL, USA
S. Kristian Hill
Affiliation:
Department of Psychology, Rosalind Franklin University of Medicine and Science, Chicago, IL, USA
John A. Sweeney
Affiliation:
Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, OH, USA
Brett A. Clementz
Affiliation:
Departments of Psychology & Neuroscience, University of Georgia, Athens, GA, USA
Jennifer E. McDowell*
Affiliation:
Departments of Psychology & Neuroscience, University of Georgia, Athens, GA, USA
*
Author for correspondence: Jennifer E. McDowell, E-mail: jemcd@uga.edu

Abstract

Background

Antisaccade tasks can be used to index cognitive control processes, e.g. attention, behavioral inhibition, working memory, and goal maintenance in people with brain disorders. Though diagnoses of schizophrenia (SZ), schizoaffective (SAD), and bipolar I with psychosis (BDP) are typically considered to be distinct entities, previous work shows patterns of cognitive deficits differing in degree, rather than in kind, across these syndromes.

Methods

Large samples of individuals with psychotic disorders were recruited through the Bipolar-Schizophrenia Network on Intermediate Phenotypes 2 (B-SNIP2) study. Anti- and pro-saccade task performances were evaluated in 189 people with SZ, 185 people with SAD, 96 people with BDP, and 279 healthy comparison participants. Logistic functions were fitted to each group's antisaccade speed-performance tradeoff patterns.

Results

Psychosis groups had higher antisaccade error rates than the healthy group, with SZ and SAD participants committing 2 times as many errors, and BDP participants committing 1.5 times as many errors. Latencies on correctly performed antisaccade trials in SZ and SAD were longer than in healthy participants, although error trial latencies were preserved. Parameters of speed-performance tradeoff functions indicated that compared to the healthy group, SZ and SAD groups had optimal performance characterized by more errors, as well as less benefit from prolonged response latencies. Prosaccade metrics did not differ between groups.

Conclusions

With basic prosaccade mechanisms intact, the higher speed-performance tradeoff cost for antisaccade performance in psychosis cases indicates a deficit that is specific to the higher-order cognitive aspects of saccade generation.

Type
Original Article
Copyright
Copyright © The Author(s) 2021. Published by Cambridge University Press

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References

American Psychiatric Association (2000). Diagnostic criteria from DSM-IV-TR. Washington, D.C.: The Association.Google Scholar
Barrett, S. L., Bell, R., Watson, D., & King, D. J. (2004). Effects of amisulpride, risperidone and chlorpromazine on auditory and visual latent inhibition, prepulse inhibition, executive function and eye movements in healthy volunteers. Journal of Psychopharmacology, 18(2), 156172. doi:10.1177/0269881104042614.CrossRefGoogle ScholarPubMed
Berg, J. L., Durant, J., Banks, S. J., & Miller, J. B. (2016). Estimates of premorbid ability in a neurodegenerative disease clinic population: Comparing the test of premorbid functioning and the wide range achievement test, 4th edition. The Clinical Neuropsychologist, 30(4), 547557. doi:10.1080/13854046.2016.1186224.CrossRefGoogle Scholar
Birchwood, M., Smith, J., Cochrane, R., Wetton, S., & Copestake, S. (1990). The social functioning scale. The development and validation of a new scale of social adjustment for use in family intervention programmes with schizophrenic patients. The British Journal of Psychiatry, 157, 853859. doi:10.1192/bjp.157.6.853.CrossRefGoogle ScholarPubMed
Clementz, B. A. (2020). Time for change in psychosis research. In Tamminga, C., Ivleva, E., Reininghaus, U., & van Os, J. (Eds.), Psychotic disorders: Comprehensive conceptualization and treatments (Vol. 83(S), pp. S72-S72). Oxford University Press.Google Scholar
Clementz, B. A., Sweeney, J. A., Hamm, J. P., Ivleva, E. I., Ethridge, L. E., Pearlson, G. D., … Tamminga, C. A. (2016). Identification of distinct psychosis biotypes using brain-based biomarkers. American Journal of Psychiatry, 173(4), 373384. doi:10.1176/appi.ajp.2015.14091200.CrossRefGoogle ScholarPubMed
Coe, B. C., & Munoz, D. P. (2017). Mechanisms of saccade suppression revealed in the anti-saccade task. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1718), 110. doi: 10.1098/rstb.2016.0192.CrossRefGoogle ScholarPubMed
Dukart, J., Schroeter, M. L., Mueller, K., & Alzheimer's Disease Neuroimaging, I. (2011). Age correction in dementia--matching to a healthy brain. PLoS One, 6(7), e22193. doi:10.1371/journal.pone.0022193.CrossRefGoogle ScholarPubMed
Egeland, J., Holmen, T. L., Bang-Kittilsen, G., Bigseth, T. T., & Engh, J. A. (2018). Category fluency in schizophrenia: Opposing effects of negative and positive symptoms? Cognitive Neuropsychiatry, 23(1), 2842. doi:10.1080/13546805.2017.1418306.CrossRefGoogle ScholarPubMed
Ethridge, L. E., Soilleux, M., Nakonezny, P. A., Reilly, J. L., Hill, S. K., Keefe, R. S., … Sweeney, J. A. (2014). Behavioral response inhibition in psychotic disorders: Diagnostic specificity, familiality and relation to generalized cognitive deficit. Schizophrenia Research, 159(2–3), 491498. doi: 10.1016/j.schres.2014.08.025.CrossRefGoogle ScholarPubMed
Ettinger, U., Ffytche, D. H., Kumari, V., Kathmann, N., Reuter, B., Zelaya, F., & Williams, S. C. (2008). Decomposing the neural correlates of antisaccade eye movements using event-related FMRI. Cerebral Cortex, 18(5), 11481159. doi:10.1093/cercor/bhm147.CrossRefGoogle ScholarPubMed
Gooding, D. C., Mohapatra, L., & Shea, H. B. (2004). Temporal stability of saccadic task performance in schizophrenia and bipolar patients. Psychological Medicine, 34(5), 921932. doi: 10.1017/s003329170300165x.CrossRefGoogle ScholarPubMed
Gooding, D. C., & Tallent, K. A. (2001). The association between antisaccade task and working memory task performance in schizophrenia and bipolar disorder. The Journal of Nervous and Mental Disease, 189(1), 816. doi:10.1097/00005053-200101000-00003.CrossRefGoogle ScholarPubMed
Gotra, M. Y., Hill, S. K., Gershon, E. S., Tamminga, C. A., Ivleva, E. I., Pearlson, G. D., … Keedy, S. K. (2020). Distinguishing patterns of impairment on inhibitory control and general cognitive ability among bipolar with and without psychosis, schizophrenia, and schizoaffective disorder. Schizophrenia Research, 223, 148157. doi: 10.1016/j.schres.2020.06.033..CrossRefGoogle ScholarPubMed
Grant, P. M., & Beck, A. T. (2009). Defeatist beliefs as a mediator of cognitive impairment, negative symptoms, and functioning in schizophrenia. Schizophrenia Bulletin, 35(4), 798806. doi:10.1093/schbul/sbn008.CrossRefGoogle Scholar
Green, M. F. (1996). What are the functional consequences of neurocognitive deficits in schizophrenia? American Journal of Psychiatry, 153(3), 321330. doi:10.1176/ajp.153.3.321.Google Scholar
Harris, M. S., Reilly, J. L., Keshavan, M. S., & Sweeney, J. A. (2006). Longitudinal studies of antisaccades in antipsychotic-naive first-episode schizophrenia. Psychological Medicine, 36(4), 485494. doi:10.1017/S0033291705006756.CrossRefGoogle ScholarPubMed
Harris, M. S., Reilly, J. L., Thase, M. E., Keshavan, M. S., & Sweeney, J. A. (2009). Response suppression deficits in treatment-naive first-episode patients with schizophrenia, psychotic bipolar disorder and psychotic major depression. Psychiatry Research, 170(2–3), 150156. doi:10.1016/j.psychres.2008.10.031.CrossRefGoogle ScholarPubMed
Helminski, J. O., & Segraves, M. A. (2003). Macaque frontal eye field input to saccade-related neurons in the superior colliculus. Journal of Neurophysiology, 90(2), 10461062. doi:10.1152/jn.00072.2003.CrossRefGoogle ScholarPubMed
Hill, S. K., Reilly, J. L., Keefe, R. S., Gold, J. M., Bishop, J. R., Gershon, E. S., … Sweeney, J. A. (2013). Neuropsychological impairments in schizophrenia and psychotic bipolar disorder: Findings from the bipolar-schizophrenia network on intermediate phenotypes (B-SNIP) study. American Journal of Psychiatry, 170(11), 12751284. doi:10.1176/appi.ajp.2013.12101298.CrossRefGoogle ScholarPubMed
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261276. doi:10.1093/schbul/13.2.261.CrossRefGoogle Scholar
Keefe, R. S., Goldberg, T. E., Harvey, P. D., Gold, J. M., Poe, M. P., & Coughenour, L. (2004). The brief assessment of cognition in schizophrenia: Reliability, sensitivity, and comparison with a standard neurocognitive battery. Schizophrenia Research, 68(2–3), 283297. doi:10.1016/j.schres.2003.09.011.CrossRefGoogle ScholarPubMed
Kimmig, H., Greenlee, M. W., Gondan, M., Schira, M., Kassubek, J., & Mergner, T. (2001). Relationship between saccadic eye movements and cortical activity as measured by fMRI: Quantitative and qualitative aspects. Experimental Brain Research, 141(2), 184194. doi:10.1007/s002210100844.CrossRefGoogle ScholarPubMed
Knox, P. C., & Pasunuru, N. (2020). Age-related alterations in inhibitory control investigated using the minimally delayed oculomotor response task. PeerJ, 8, e8401. doi:10.7717/peerj.8401.CrossRefGoogle ScholarPubMed
Lambert, Z. V., Wildt, A. R., & Durand, R. M. (1988). Redundancy analysis: An alternative to canonical correlation and multivariate multiple regression in exploring interset associations. Psychological Bulletin, 104(2), 282289.CrossRefGoogle Scholar
Li, Q., Amlung, M. T., Valtcheva, M., Camchong, J., Austin, B. P., Dyckman, K. A., … McDowell, J. E. (2012). Evidence from cluster analysis for differentiation of antisaccade performance groups based on speed/accuracy trade-offs. International Journal of Psychophysiology, 85(2), 274277. doi:10.1016/j.ijpsycho.2012.03.008.CrossRefGoogle ScholarPubMed
Lui, S., Yao, L., Xiao, Y., Keedy, S. K., Reilly, J. L., Keefe, R. S., … Sweeney, J. A. (2015). Resting-state brain function in schizophrenia and psychotic bipolar probands and their first-degree relatives. Psychological Medicine, 45(1), 97108. doi:10.1017/S003329171400110X.CrossRefGoogle ScholarPubMed
Luna, B., Thulborn, K. R., Strojwas, M. H., McCurtain, B. J., Berman, R. A., Genovese, C. R., & Sweeney, J. A. (1998). Dorsal cortical regions subserving visually guided saccades in humans: An fMRI study. Cerebral Cortex (New York, N.Y.: 1991), 8(1), 4047. doi:10.1093/cercor/8.1.40.CrossRefGoogle Scholar
Luna, B., Velanova, K., & Geier, C. F. (2008). Development of eye-movement control. Brain and Cognition, 68(3), 293308. doi:10.1016/j.bandc.2008.08.019.CrossRefGoogle ScholarPubMed
Matzke, D., Love, J., & Heathcote, A. (2017). A Bayesian approach for estimating the probability of trigger failures in the stop-signal paradigm. Behavior Research Methods, 49(1), 267281. doi:10.3758/s13428-015-0695-8.CrossRefGoogle ScholarPubMed
McDowell, J. E., Dyckman, K. A., Austin, B. P., & Clementz, B. A. (2008). Neurophysiology and neuroanatomy of reflexive and volitional saccades: Evidence from studies of humans. Brain and Cognition, 68(3), 255270. doi:10.1016/j.bandc.2008.08.016.CrossRefGoogle ScholarPubMed
McPeek, R. M., & Keller, E. L. (2004). Deficits in saccade target selection after inactivation of superior colliculus. Nature Neuroscience, 7(7), 757763. doi:10.1038/nn1269.CrossRefGoogle ScholarPubMed
Montgomery, S. A., & Asberg, M. (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry, 134, 382389. doi:10.1192/bjp.134.4.382.CrossRefGoogle ScholarPubMed
Peck, C. K. (1990). Neuronal activity related to head and eye movements in cat superior colliculus. The Journal of Physiology, 421, 79104. doi:10.1113/jphysiol.1990.sp017934.CrossRefGoogle ScholarPubMed
Pierce, J. E., & McDowell, J. E. (2016). Modulation of cognitive control levels via manipulation of saccade trial-type probability assessed with event-related BOLD fMRI. Journal of Neurophysiology, 115(2), 763772. doi: 10.1152/jn.00776.2015.CrossRefGoogle ScholarPubMed
Polli, F. E., Barton, J. J., Vangel, M., Goff, D. C., Iguchi, L., & Manoach, D. S. (2006). Schizophrenia patients show intact immediate error-related performance adjustments on an antisaccade task. Schizophrenia Research, 82(2–3), 191201. doi:10.1016/j.schres.2005.10.003.CrossRefGoogle Scholar
Radant, A. D., Dobie, D. J., Calkins, M. E., Olincy, A., Braff, D. L., Cadenhead, K. S., … Tsuang, D. W. (2010). Antisaccade performance in schizophrenia patients, their first-degree biological relatives, and community comparison subjects: Data from the COGS study. Psychophysiology, 47(5), 846856. doi:10.1111/j.1469-8986.2010.01004.x.Google ScholarPubMed
Radant, A. D., Millard, S. P., Braff, D. L., Calkins, M. E., Dobie, D. J., Freedman, R., … Tsuang, D. W. (2015). Robust differences in antisaccade performance exist between COGS schizophrenia cases and controls regardless of recruitment strategies. Schizophrenia Research, 163(1–3), 4752. doi:10.1016/j.schres.2014.12.016.CrossRefGoogle ScholarPubMed
Rector, N. A., Beck, A. T., & Stolar, N. (2005). The negative symptoms of schizophrenia: A cognitive perspective. The Canadian Journal of Psychiatry, 50(5), 247257. doi:10.1177/070674370505000503.CrossRefGoogle ScholarPubMed
Reilly, J. L., Frankovich, K., Hill, S., Gershon, E. S., Keefe, R. S., Keshavan, M. S., … Sweeney, J. A. (2014). Elevated antisaccade error rate as an intermediate phenotype for psychosis across diagnostic categories. Schizophrenia Bulletin, 40(5), 10111021. doi:10.1093/schbul/sbt132.CrossRefGoogle ScholarPubMed
Reilly, J. L., Harris, M. S., Khine, T. T., Keshavan, M. S., & Sweeney, J. A. (2008). Reduced attentional engagement contributes to deficits in prefrontal inhibitory control in schizophrenia. Biological Psychiatry, 63(8), 776783. doi:10.1016/j.biopsych.2007.11.009.CrossRefGoogle Scholar
Richter, S. J., & McCann, M. H. (2012). Using the Tukey-Kramer omnibus test in the Hayter-Fisher procedure. British Journal of Mathematical and Statistical Psychology, 65(3), 499510. doi:10.1111/j.2044-8317.2012.02041.x.CrossRefGoogle ScholarPubMed
Schiller, P. H., Sandell, J. H., & Maunsell, J. H. (1987). The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. Journal of Neurophysiology, 57(4), 10331049. doi:10.1152/jn.1987.57.4.1033.CrossRefGoogle ScholarPubMed
Sereno, A. B., Briand, K. A., Amador, S. C., & Szapiel, S. V. (2006). Disruption of reflexive attention and eye movements in an individual with a collicular lesion. Journal of Clinical and Experimental Neuropsychology, 28(1), 145166. doi:10.1080/13803390590929298.CrossRefGoogle Scholar
Shafiq-Antonacci, R., Maruff, P., Whyte, S., Tyler, P., Dudgeon, P., & Currie, J. (1999). The effects of age and mood on saccadic function in older individuals. The Journals of Gerontology, Series B: Psychological Sciences and Social Sciences, 54(6), P361P368. doi:10.1093/geronb/54b.6.p361.CrossRefGoogle ScholarPubMed
Tamminga, C. A., Ivleva, E. I., Keshavan, M. S., Pearlson, G. D., Clementz, B. A., Witte, B., … Sweeney, J. A. (2013). Clinical phenotypes of psychosis in the bipolar-schizophrenia network on intermediate phenotypes (B-SNIP). American Journal of Psychiatry, 170(11), 12631274. doi:10.1176/appi.ajp.2013.12101339.CrossRefGoogle Scholar
Tien, A. Y., Ross, D. E., Pearlson, G., & Strauss, M. E. (1996). Eye movements and psychopathology in schizophrenia and bipolar disorder. The Journal of Nervous and Mental Disease, 184(6), 331338. doi: 10.1097/00005053-199606000-00001.CrossRefGoogle ScholarPubMed
Unsworth, N., Schrock, J. C., & Engle, R. W. (2004). Working memory capacity and the antisaccade task: Individual differences in voluntary saccade control. Journal of Experimental Psychology: Learning, Memory, and Cognition, 30(6), 13021321. doi:10.1037/0278-7393.30.6.1302.Google ScholarPubMed
Young, R. C., Biggs, J. T., Ziegler, V. E., & Meyer, D. A. (1978). A rating scale for mania: Reliability, validity and sensitivity. British Journal of Psychiatry, 133, 429435. doi:10.1192/bjp.133.5.429.CrossRefGoogle ScholarPubMed
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