Attentional M100 gain modulation localizes to auditory sensory cortex and is deficient in first‐episode psychosis

Abstract

Selective attention is impaired in first‐episode psychosis (FEP). Selective attention effects can be detected during auditory tasks as increased sensory activity. We previously reported electroencephalography scalp‐measured N100 enhancement is reduced in FEP. Here, we localized magnetoencephalography (MEG) M100 source activity within the auditory cortex, making novel use of the Human Connectome Project multimodal parcellation (HCP‐MMP) to identify precise auditory cortical areas involved in attention modulation and its impairment in FEP. MEG was recorded from 27 FEP and 31 matched healthy controls (HC) while individuals either ignored frequent standard and rare oddball tones while watching a silent movie or attended tones by pressing a button to oddballs. Because M100 arises mainly in the auditory cortices, MEG activity during the M100 interval was projected to the auditory sensory cortices defined by the HCP‐MMP (A1, lateral belt, and parabelt parcels). FEP had less auditory sensory cortex M100 activity in both conditions. In addition, there was a significant interaction between group and attention. HC enhanced source activity with attention, but FEP did not. These results demonstrate deficits in both sensory processing and attentional modulation of the M100 in FEP. Novel use of the HCP‐MMP revealed the precise cortical areas underlying attention modulation of auditory sensory activity in healthy individuals and impairments in FEP. The sensory reduction and attention modulation impairment indicate local and systems‐level pathophysiology proximal to disease onset that may be critical for etiology. Further, M100 and N100 enhancement may serve as outcome variables for targeted intervention to improve attention in early psychosis.

Functional connectivity and gray matter deficits within the auditory attention circuit in first-episode psychosis

“…This study included the same participants as Curtis and colleagues ( 9 ), comprising 27 FEP (recruited from Western Psychiatric Hospital with <2 months lifetime antipsychotic exposure) and 31 healthy controls (HC). No participant had a history of concussion or head injury with sequelae, history of alcohol or drug addiction or detox in the last 5 years, or neurological comorbidity.…”

“…MRI acquisition and processing steps were the same as Curtis and colleagues ( 9 ). The following data were acquired on a Siemens 3T MAGNETOM Prisma scanner using a 32-channel phase array head coil: A single-band reference image with no slice acceleration at the beginning of each run; T1-weighted 3D MPRAGE images (TR/TE/TI = 2400/2.22/1000 ms, flip angle = 7°, FOV = 256 × 240mm, voxel size = 0.8 mm 3 , 208 slices, GRAPPA acceleration factor = 2); T2-SPACE images (TR = 3,200 ms TE = 563 ms, FOV = 256 × 240, voxel size = 0.8 mm 3 , 208 slices); A fieldmap (TR = 731 ms, TE = 4.92/7.38 ms, FOV = 208 × 180, voxel size = 2.0 mm 3 voxel size, 72 slices); Ten minutes eyes-open, resting BOLD fMRI multiband data (TR = 800 ms, TE = 37 ms, multiband factor = 8, flip angle = 52°, FOV = 208 × 208mm, voxel size = 2.0 mm 3 , 72 slices); and Spin echo EPI images with reversed phase encoding directions (TR = 8,000 ms, TE = 66 ms, flip angle = 90°, FOV = 208 × 208mm, voxel size = 2.0 mm 3 , 72 slices).…”

“…MRI acquisition and processing steps were the same as Curtis and colleagues (9). The following data were acquired on a Siemens 3T MAGNETOM Prisma scanner using a 32-channel phase array head coil: A single-band reference image with no slice acceleration at the beginning of each run; T1-weighted 3D MPRAGE images (TR/TE/ TI = 2400/2.…”

“…The EEG-measured auditory event-related potential (or MEG-measured event-related field) ~100 ms post-stimulus (N100/M100) is enhanced with attention in healthy individuals but not in schizophrenia or first episode psychosis (FEP) (5)(6)(7)(8). We recently showed that FEP have reduced M100 modulation by attention in primary auditory cortex, lateral belt, and parabelt (9). However, it is unclear if the pathology underlying this impairment is restricted to mechanisms within auditory sensory cortex or involves non-auditory executive control regions as well.…”

“…The current study is a follow-up to our recent report that identified M100 attention modulation deficits in auditory cortex in FEP (9). To investigate functional and structural deficits in local and long-range networks underlying the M100 attentional modulation deficit in FEP, we used a multi-stepped strategy.…”