Demand and modality of directed attention modulate "pre-attentive" sensory processes in schizophrenia patients and nonpsychiatric controls

Abstract

Background: Mismatch negativity (MNN) and P3a are event related potential (ERP) measures of early sensory information processing. These components are usually conceptualized as being "pre-attentive" and therefore immune to changes with variations in attentional functioning. This study aimed to determine whether manipulations of attention influence the amplitudes and latencies of MMN and P3a and, if so, the extent to which these early sensory processes govern concurrent behavioral vigilance performance in schizophrenia patients and normal subjects.

Methods: Schizophrenia patients (SZ; n = 20) and Nonpsychiatric Control Subjects (NCS; n = 20) underwent auditory ERP testing to assess MMN and P3a across 4 EEG recording sessions in which attentional demand (low vs. high) and sensory modality of directed attention (visual vs. auditory) were experimentally varied.

Results: Across conditions, SZ patients exhibited deficits in MMN and P3a amplitudes. Significant amplitude and latency modulation were observed in both SZ and NCS but there were no group-by-condition interactions. The amount of MMN amplitude attenuation from low- to high-demand tasks was significantly associated with increased vigilance performance in both SZ and NCS groups (r = -0.67 and r = -0.60). Several other robust associations were also observed among neurophysiologic, clinical and cognitive variables.

Conclusions: Attentional demand and modality of directed attention significantly influence the amplitude and latencies of "pre-attentive" ERP components in both SZ and NCS. Deficits in MMN and P3a were not "normalized" when attention was directed to the auditory stimuli in schizophrenia patients. The adaptive modulation of early sensory information processing appears to govern concurrent attentional task performance. The temporal window reflecting automatic sensory discrimination as indexed as MMN and P3a may serve as a gateway to some higher order cognitive operations necessary for psychosocial functioning.

Figure 1. Experimental Design

Figure depicts the visual and auditory stimuli across tasks and stimulus types. The arrows denote modality of directed attention with number of arrows indicating attentional demand (low- vs. high-demand). Auditory stimuli included standard (S), duration deviant (D), and white noise (WN) stimuli. Average MMN and P3a ERP responses to nontarget stimuli from the Fz electrode site are shown for Schizophrenia Patients (red) and Healthy Controls C (blue) subjects. Scalp topography maps for MMN and P3a at each group is also provided.

Figure 2. MMN and P3a event-related potentials across tasks

Schizophrenia patients exhibited robust deficits across tasks. Main effects of task paradigm were present, demonstrating significant amplitude and latency modulation across tasks. For example, significant MMN amplitude reductions were present when subjects completed the high-demand visual CPT task (shaded region). In contrast, MMN amplitudes in the passive video and auditory target detection task were not significantly different. When attention was directed to the auditory stimuli, MMN and P3a latencies were significantly prolonged relative to the other task paradigms (shown by brackets). No group-by-task paradigm interactions were present, indicating that schizophrenia patients exhibited normal amplitude and latency modulation across tasks.

Figure 3. MMN and P3a amplitude and latency modulation at electrode Fz across task paradigms

Significant main effects of group were present, indicating amplitude deficits in schizophrenia patients. Main effects of task paradigm were present, demonstrating significant amplitude and latency modulation. Significant latency main effects were present with increased latencies to non-target stimuli when attention was directed to the auditory stimuli. Latencies were prolonged by 13-16 msec for MMN and 29-32 msec for P3a. No group-by-task paradigm interactions were present, indicating that schizophrenia patients exhibited normal amplitude and latency modulation across tasks. Note: * indicates a significant group difference.

Figure 4

Across groups, MMN responses were larger under conditions with low vs. high task demand with no group by demand interaction. In contrast, P3a responses were larger in the high attentional demand conditions with no group by demand interaction. For both MMN and P3a, amplitudes were larger when attention was directed to the auditory vs. visual modality with no group by modality interaction. Note: * indicates a significant effect of modality and significant effect of task demand.

Figure 5

Schizophrenia patients exhibited deficits in reaction time and sensitivity (d’) in both the visual and auditory modalities. Expected patterns of performance decrement were observed with increasing task difficulty in both modalities of attention and both groups. Behavioral discriminability was greater for the easier-to-detect WN vs. DD stimuli across both groups.

Figure 6. Attentional modulation of MMN is associated with behavioral attentional performance

Amount of MMN modulation (low- minus high-demand visual directed attention tasks) in response to WN stimuli is significantly correlated with CPT-IP behavioral performance in both schizophrenia patients and controls. Both groups exhibit shifts of processing resources from pre- to post-attentive levels of processing with increasing attentional demands. This pre- attentional ERP amplitude tradeoff (i.e., attenuation) was present in both groups. Subjects with a greater reduction in MMN amplitude with increased visual task demands had better CPT-IP attentional functioning.