Intersensory attention deficits in schizophrenia relate to ongoing sensorimotor beta oscillations

Abstract

This study tested whether intersensory attention deficits in people with schizophrenia (SZ) relate to aberrant ongoing oscillations in sensory cortices. Electroencephalography (EEG) was recorded while individuals with schizophrenia (N = 27) and healthy controls (HC; N = 27) performed a visual-tactile target detection task. Ongoing alpha (8-12 Hz) and lower beta (13-20 Hz) band oscillations in visual and sensorimotor cortices were examined. Behavioral data suggested an intersensory attention deficit in patients. EEG data revealed stronger alpha-band oscillations for tactile vs. visual attention conditions in the visual cortex of both study groups. In the sensorimotor cortex contralateral to the tactile stimulation site, patients showed an additional intersensory attention effect in ongoing beta-band oscillations, which was negatively related to cognitive and positive symptoms of the PANSS. Our findings extend previous results from unisensory attention research and suggest that deficits in intersensory attention and alterations in sensorimotor beta oscillations are related to schizophrenia symptomatology.

Fig. 1. Setup of the intersensory attention paradigm and stimulation stream.

Left panel: Setup of the study. The tilted monitor enabled simultaneous and spatially aligned presentation of visual stimuli (central location on the screen) and tactile stimuli (presented via a Braille-stimulator placed on the back of the screen and applied to the index finger of the left hand). Muscle fatigue was prevented by cushioning the left hand. Behavioral responses were given by the index finger of the right hand. Right panel: Stimulation stream comprising of unisensory visual, unisensory tactile and bisensory visuotactile standard and target stimuli, which were presented in random order. Participants attended to either visual or tactile input, pressing the response button when the occasional target stimulus in the attended sensory modality appeared.

Fig. 2. Virtual electrodes with the corresponding nodes (dots) for each of the three VOIs.

From left to right: left sensorimotor hand region, right sensorimotor hand region (each with 3 nodes), viewed from axial plane, and primary visual region (11 nodes), left posterior view.

Fig. 3. Behavioral results for d-prime values and reaction times.

a Behavioral data showing deficits in IA for unisensory visual and unisensory tactile stimuli but not bisensory VT stimuli. The figure contrasts individuals with SZ (SZ, turquoise dots) and HC (red dots). Unisensory deficits were present in both visual and tactile attention conditions. There was an overall better performance for bisensory stimuli than for unisensory stimuli across groups and sensory modalities. People with SZ performed worse than HC specifically on the unisensory stimuli, whereas there were no significant performance differences on bisensory stimuli. b Behavioral data showing RT differences for bisensory vs. unisensory stimuli. In the attend-tactile blocks, differences between bisensory and unisensory stimuli were found, with bisensory stimuli showing faster RTs than unisensory tactile stimuli. This was not apparent for the attend-visual blocks. The large dots represent mean values with the error bars representing ± 1SE. The smaller dots represent individual datapoints. Significant main effects and interactions are represented with asterisks (n.s, p > 0.05, *p < 0.05, **p < 0.01).

Fig. 4. Topographical plots of alpha band and beta band activity at the surface electrode level.

Plots show alpha (left) and beta (right) power for HZ and individuals with SZ for each attention condition as well as the relative percent difference between visual and tactile attention conditions.

Fig. 5. Ongoing alpha (8-12 Hz) and beta (12–20 Hz) power in the control group.

Left panel: The control group showed the predicted stronger alpha power in the visual cortex when attention was directed to tactile compared to when it was directed to visual stimuli VOI (left panel). This was the case for when one outlier value was removed. Right panel: There were no significant attention effects on beta power (after removing one outlier value). The small arrows with asterisks represent Bonferroni-corrected follow-up contrasts between the attention conditions, *p < 0.05, **p < 0.01,***p < 0.001 n.s. = non-significant.

Fig. 6. Ongoing alpha (8-12 Hz) and beta (13–20 Hz) oscillations are altered in people with SZ relative to HC participants.

a Time-frequency representations for the occipital VOI (left), left sensorimotor VOI (middle), the right sensorimotor VOI (right), showing visual-attention (V) and tactile-attention (T) conditions and the contrast between conditions. b Alpha (left) and beta (right) power for both study groups (HC, red, and SZ turquoise). The y-axis scale represents the relative percentage change between conditions, i.e., (V – T)/T * 100. Values below zero represents a relatively stronger power in attend-tactile condition, whereas a difference above zero represents a stronger power in attend-visual condition. Individual points represent participants, large dots show mean with ± 1 SE CI. The purple box highlights the significant Group*VOI interaction for beta power in the right sensorimotor VOI, **p < 0.01.

Fig. 7. Multivariate multiple linear regression of PANSS dimensions with IA effects on right sensorimotor beta power in patients with SZ.

The analysis revealed that a stronger IA effect (i.e. higher beta activity in the non-attended condition) was associated with lower SZ symptomatology in the positive and cognitive dimensions of the PANSS. Other dimensions (in gray) were not significantly predicted by relative beta power change.