Impaired Filtering and Hyperfocusing: Neural Evidence for Distinct Selective Attention Abnormalities in People with Schizophrenia

Abstract

Although schizophrenia is classically thought to involve impaired attentional filtering, people with schizophrenia (PSZ) exhibit a more intense and more exclusive attentional focus than healthy control subjects (HCS) in many tasks. To resolve this contradiction, this functional magnetic resonance imaging study tested the impact of attentional control demands on the modulation of stimulus-induced activation in the fusiform face area and parahippocampal place area when participants (43 PSZ and 43 HCS) were looking for a target face versus house. Stimuli were presented individually, or as face-house overlays that challenged attentional control. Responses were slower for house than face stimuli and when prioritizing houses over faces in overlays, suggesting a difference in salience. Blood-oxygen-level-dependent activity reflected poorer attentional selectivity in PSZ than HCS when attentional control was challenged most, that is, when stimuli were overlaid and the task required detecting the lower-salience house target. By contrast, attentional selectivity was exaggerated in PSZ when control was challenged least, that is, when stimuli were presented sequentially and the task required detecting the higher-salience face target. These findings are consistent with 2 distinct attentional abnormalities in schizophrenia leading to impaired and exaggerated selection under different conditions: attentional control deficits, and hyperfocusing once attention has been directed toward a stimulus.

Keywords: Cognitive; functional magnetic resonance imaging; fusiform face area; parahippocampal place area; psychosis.

Figure 1

An example of a task block in the Sequential condition (top) and in the Overlay condition (bottom). Stimuli are shown to size relative to the whole screen display. The text on the initial instruction screen reads “If the face [house] onscreen matches this face [house], press with your index finger. For all other images, press with your middle finger.” The screen background of the initial instruction screen was cyan, all other colors are as presented in the real task.

Figure 2

FFA and PPA activation in face blocks and house blocks of the functional localizer. Signal change is relative to passive fixation. Bars represent the mean over 41 HCS and 42 PSZ. Error bars represent the standard error of the mean (SEM).

Figure 3

Percentage of BOLD signal change in the FFA and PPA induced by face and house images in the Sequential condition of the attention task, averaged over attended stimulus dimension, at each of 17 measurement time points. A measurement was taken every 780 ms. The graph represents averages (±SEM) over 41 HCS and 42 PSZ.

Figure 4

Behavioral task performance in the Sequential condition. (a) Hit rate (% correct detections) and RT of responses to the target stimulus of the to-be-attended dimension. (b) False alarm rate (% incorrect “target” responses) and RT of responses to the irrelevant target stimulus, that is, the target stimulus of the not-to-be-attended dimension. (c) False alarm rate and RT of responses to nontarget stimuli. Bars reflect the mean (±SEM) over 41 HCS and 42 PSZ.

Figure 5

BOLD signal change in the Sequential condition in the FFA in response to face images (top panels) and in the PPA in response to house images (bottom panels) as a function of whether participants were looking for the target face or the target house. A measurement was taken every 780 ms. Measurement timepoints within the gray area entered statistical analysis of response amplitude. Each represented datapoint reflects the mean (±SEM) over 41 HCS and 42 PSZ.

Figure 6

Behavioral task performance in the Overlay condition. (a) Hit rate and RT of responses to stimuli containing the target image of the to-be-attended dimension. (b) False alarm rate (% of incorrect “target” responses) and RT of responses to stimuli containing the irrelevant target stimulus, that is, the target stimulus of the not-to-be-attended dimension. (c) False alarm rate and RT of responses to nontarget stimuli. Bars reflect the mean (±SEM) over 41 HCS and 42 PSZ.

Figure 7

BOLD signal response to overlay stimuli in the FFA (top panels) and in the PPA (bottom panels) as a function of whether participants were looking for the target face or the target house. A measurement was taken every 780 ms. Measurement timepoints within the gray area entered statistical analysis of response amplitude. Each represented datapoint reflects the mean (±SEM) over 41 HCS and 42 PSZ.