Aberrant Cortical Connectivity During Ambiguous Object Recognition Is Associated With Schizophrenia

Victor J Pokorny; Tori Espensen-Sturges; Philip C. Burton; Scott R. Sponheim; Cheryl A. Olman

doi:10.1016/j.bpsc.2020.09.018

Aberrant Cortical Connectivity During Ambiguous Object Recognition Is Associated With Schizophrenia

Victor J Pokorny, Tori Espensen-Sturges, Philip C. Burton, Scott R. Sponheim, Cheryl A. Olman

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

Background: Dysfunctional connectivity within the perceptual hierarchy is proposed to be an integral component of psychosis. The fragmented ambiguous object task was implemented to investigate neural connectivity during object recognition in patients with schizophrenia (SCZ) and bipolar disorder and first-degree relatives of patients with SCZ (SREL). Methods: We analyzed 3T functional magnetic resonance imaging data collected from 27 patients with SCZ, 23 patients with bipolar disorder, 24 control subjects, and 19 SREL during the administration of the fragmented ambiguous object task. Fragmented ambiguous object task stimuli were line-segmented versions of objects and matched across a number of low-level features. Images were categorized as meaningful or meaningless based on ratings assigned by the participants. Results: An a priori region of interest was defined in the primary visual cortex (V1). In addition, the lateral occipital complex/ventral visual areas, intraparietal sulcus (IPS), and middle frontal gyrus (MFG) were identified functionally via the contrast of cortical responses to stimuli judged as meaningful or meaningless. SCZ was associated with altered neural activations at V1, IPS, and MFG. Psychophysiological interaction analyses revealed negative connectivity between V1 and MFG in patient groups and altered modulation of connectivity between conditions from right IPS to left IPS and right IPS to left MFG in patients with SCZ and SREL. Conclusions: Results provide evidence that SCZ is associated with inefficient processing of ambiguous visual objects at V1, which is likely attributable to altered feedback from higher-level visual areas. We also observed distinct patterns of aberrant connectivity among low-level, mid-level, and high-level visual areas in patients with SCZ, patients with bipolar disorder, and SREL.

Original language	English (US)
Pages (from-to)	1193-1201
Number of pages	9
Journal	Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume	6
Issue number	12
DOIs	https://doi.org/10.1016/j.bpsc.2020.09.018
State	Published - Dec 2021

Bibliographical note

Funding Information:
This work was supported by the awards by the Department of Veterans Affairs Clinical Science Research and Development Service (Grant No. I01CX000227 [to SRS]) and the National Institute of Mental Health of the National Institutes of Health (NIH) (Grant No. R01MH112583 [to SRS]). This work is also supported by the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. P30 NS076408 ), the National Eye Institute of the NIH (Grant No. P30 EY011374 ), the National Institute of Biomedical Imaging and Bioengineering of the NIH (Grant No. P41EB015894 ), and the NIH (Grant No. 1S10OD017974-01 ). The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Veterans Affairs or the NIH.

Funding Information:
This work was supported by the awards by the Department of Veterans Affairs Clinical Science Research and Development Service (Grant No. I01CX000227 [to SRS]) and the National Institute of Mental Health of the National Institutes of Health (NIH) (Grant No. R01MH112583 [to SRS]). This work is also supported by the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. P30 NS076408), the National Eye Institute of the NIH (Grant No. P30 EY011374), the National Institute of Biomedical Imaging and Bioengineering of the NIH (Grant No. P41EB015894), and the NIH (Grant No. 1S10OD017974-01). The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Veterans Affairs or the NIH. We would like to thank Isaac Hatch-Gillette, Joseph Lupo, and Haven Hafar for their assistance with data collection and Julia Longenecker for her assistance with task development. The authors report no biomedical financial interests or potential conflicts of interest.

Publisher Copyright:
© 2020 Society of Biological Psychiatry

Keywords

Object recognition
Psychosis
Schizophrenia
Vision
fMRI

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@article{2759345d2eb944afa69332b6fd7dad1b,

title = "Aberrant Cortical Connectivity During Ambiguous Object Recognition Is Associated With Schizophrenia",

abstract = "Background: Dysfunctional connectivity within the perceptual hierarchy is proposed to be an integral component of psychosis. The fragmented ambiguous object task was implemented to investigate neural connectivity during object recognition in patients with schizophrenia (SCZ) and bipolar disorder and first-degree relatives of patients with SCZ (SREL). Methods: We analyzed 3T functional magnetic resonance imaging data collected from 27 patients with SCZ, 23 patients with bipolar disorder, 24 control subjects, and 19 SREL during the administration of the fragmented ambiguous object task. Fragmented ambiguous object task stimuli were line-segmented versions of objects and matched across a number of low-level features. Images were categorized as meaningful or meaningless based on ratings assigned by the participants. Results: An a priori region of interest was defined in the primary visual cortex (V1). In addition, the lateral occipital complex/ventral visual areas, intraparietal sulcus (IPS), and middle frontal gyrus (MFG) were identified functionally via the contrast of cortical responses to stimuli judged as meaningful or meaningless. SCZ was associated with altered neural activations at V1, IPS, and MFG. Psychophysiological interaction analyses revealed negative connectivity between V1 and MFG in patient groups and altered modulation of connectivity between conditions from right IPS to left IPS and right IPS to left MFG in patients with SCZ and SREL. Conclusions: Results provide evidence that SCZ is associated with inefficient processing of ambiguous visual objects at V1, which is likely attributable to altered feedback from higher-level visual areas. We also observed distinct patterns of aberrant connectivity among low-level, mid-level, and high-level visual areas in patients with SCZ, patients with bipolar disorder, and SREL.",

keywords = "Object recognition, Psychosis, Schizophrenia, Vision, fMRI",

author = "Pokorny, {Victor J} and Tori Espensen-Sturges and Burton, {Philip C.} and Sponheim, {Scott R.} and Olman, {Cheryl A.}",

note = "Funding Information: This work was supported by the awards by the Department of Veterans Affairs Clinical Science Research and Development Service (Grant No. I01CX000227 [to SRS]) and the National Institute of Mental Health of the National Institutes of Health (NIH) (Grant No. R01MH112583 [to SRS]). This work is also supported by the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. P30 NS076408 ), the National Eye Institute of the NIH (Grant No. P30 EY011374 ), the National Institute of Biomedical Imaging and Bioengineering of the NIH (Grant No. P41EB015894 ), and the NIH (Grant No. 1S10OD017974-01 ). The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Veterans Affairs or the NIH. Funding Information: This work was supported by the awards by the Department of Veterans Affairs Clinical Science Research and Development Service (Grant No. I01CX000227 [to SRS]) and the National Institute of Mental Health of the National Institutes of Health (NIH) (Grant No. R01MH112583 [to SRS]). This work is also supported by the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. P30 NS076408), the National Eye Institute of the NIH (Grant No. P30 EY011374), the National Institute of Biomedical Imaging and Bioengineering of the NIH (Grant No. P41EB015894), and the NIH (Grant No. 1S10OD017974-01). The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Veterans Affairs or the NIH. We would like to thank Isaac Hatch-Gillette, Joseph Lupo, and Haven Hafar for their assistance with data collection and Julia Longenecker for her assistance with task development. The authors report no biomedical financial interests or potential conflicts of interest. Publisher Copyright: {\textcopyright} 2020 Society of Biological Psychiatry",

year = "2021",

month = dec,

doi = "10.1016/j.bpsc.2020.09.018",

language = "English (US)",

volume = "6",

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AU - Pokorny, Victor J

AU - Espensen-Sturges, Tori

AU - Burton, Philip C.

AU - Sponheim, Scott R.

AU - Olman, Cheryl A.

N1 - Funding Information: This work was supported by the awards by the Department of Veterans Affairs Clinical Science Research and Development Service (Grant No. I01CX000227 [to SRS]) and the National Institute of Mental Health of the National Institutes of Health (NIH) (Grant No. R01MH112583 [to SRS]). This work is also supported by the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. P30 NS076408 ), the National Eye Institute of the NIH (Grant No. P30 EY011374 ), the National Institute of Biomedical Imaging and Bioengineering of the NIH (Grant No. P41EB015894 ), and the NIH (Grant No. 1S10OD017974-01 ). The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Veterans Affairs or the NIH. Funding Information: This work was supported by the awards by the Department of Veterans Affairs Clinical Science Research and Development Service (Grant No. I01CX000227 [to SRS]) and the National Institute of Mental Health of the National Institutes of Health (NIH) (Grant No. R01MH112583 [to SRS]). This work is also supported by the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. P30 NS076408), the National Eye Institute of the NIH (Grant No. P30 EY011374), the National Institute of Biomedical Imaging and Bioengineering of the NIH (Grant No. P41EB015894), and the NIH (Grant No. 1S10OD017974-01). The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Veterans Affairs or the NIH. We would like to thank Isaac Hatch-Gillette, Joseph Lupo, and Haven Hafar for their assistance with data collection and Julia Longenecker for her assistance with task development. The authors report no biomedical financial interests or potential conflicts of interest. Publisher Copyright: © 2020 Society of Biological Psychiatry

PY - 2021/12

Y1 - 2021/12

N2 - Background: Dysfunctional connectivity within the perceptual hierarchy is proposed to be an integral component of psychosis. The fragmented ambiguous object task was implemented to investigate neural connectivity during object recognition in patients with schizophrenia (SCZ) and bipolar disorder and first-degree relatives of patients with SCZ (SREL). Methods: We analyzed 3T functional magnetic resonance imaging data collected from 27 patients with SCZ, 23 patients with bipolar disorder, 24 control subjects, and 19 SREL during the administration of the fragmented ambiguous object task. Fragmented ambiguous object task stimuli were line-segmented versions of objects and matched across a number of low-level features. Images were categorized as meaningful or meaningless based on ratings assigned by the participants. Results: An a priori region of interest was defined in the primary visual cortex (V1). In addition, the lateral occipital complex/ventral visual areas, intraparietal sulcus (IPS), and middle frontal gyrus (MFG) were identified functionally via the contrast of cortical responses to stimuli judged as meaningful or meaningless. SCZ was associated with altered neural activations at V1, IPS, and MFG. Psychophysiological interaction analyses revealed negative connectivity between V1 and MFG in patient groups and altered modulation of connectivity between conditions from right IPS to left IPS and right IPS to left MFG in patients with SCZ and SREL. Conclusions: Results provide evidence that SCZ is associated with inefficient processing of ambiguous visual objects at V1, which is likely attributable to altered feedback from higher-level visual areas. We also observed distinct patterns of aberrant connectivity among low-level, mid-level, and high-level visual areas in patients with SCZ, patients with bipolar disorder, and SREL.

AB - Background: Dysfunctional connectivity within the perceptual hierarchy is proposed to be an integral component of psychosis. The fragmented ambiguous object task was implemented to investigate neural connectivity during object recognition in patients with schizophrenia (SCZ) and bipolar disorder and first-degree relatives of patients with SCZ (SREL). Methods: We analyzed 3T functional magnetic resonance imaging data collected from 27 patients with SCZ, 23 patients with bipolar disorder, 24 control subjects, and 19 SREL during the administration of the fragmented ambiguous object task. Fragmented ambiguous object task stimuli were line-segmented versions of objects and matched across a number of low-level features. Images were categorized as meaningful or meaningless based on ratings assigned by the participants. Results: An a priori region of interest was defined in the primary visual cortex (V1). In addition, the lateral occipital complex/ventral visual areas, intraparietal sulcus (IPS), and middle frontal gyrus (MFG) were identified functionally via the contrast of cortical responses to stimuli judged as meaningful or meaningless. SCZ was associated with altered neural activations at V1, IPS, and MFG. Psychophysiological interaction analyses revealed negative connectivity between V1 and MFG in patient groups and altered modulation of connectivity between conditions from right IPS to left IPS and right IPS to left MFG in patients with SCZ and SREL. Conclusions: Results provide evidence that SCZ is associated with inefficient processing of ambiguous visual objects at V1, which is likely attributable to altered feedback from higher-level visual areas. We also observed distinct patterns of aberrant connectivity among low-level, mid-level, and high-level visual areas in patients with SCZ, patients with bipolar disorder, and SREL.

KW - Object recognition

KW - Psychosis

KW - Schizophrenia

KW - Vision

KW - fMRI

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Aberrant Cortical Connectivity During Ambiguous Object Recognition Is Associated With Schizophrenia

Abstract

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