Brain mechanisms of involuntary visuospatial attention: an event-related potential study

Abstract

The brain mechanisms mediating visuospatial attention were investigated by recording event-related potentials (ERPs) during a line-orientation discrimination task. Nonpredictive peripheral cues were used to direct participant's attention involuntarily to a spatial location. The earliest attentional modulation was observed in the P1 component (peak latency about 130 ms), with the valid trials eliciting larger P1 than invalid trials. Moreover, the attentional modulations on both the amplitude and latency of the P1 and N1 components had a different pattern as compared to previous studies with voluntary attention tasks. In contrast, the earliest visual ERP component, C1 (peak latency about 80 ms), was not modulated by attention. Low-resolution brain electromagnetic tomography (LORETA) showed that the earliest attentional modulation occurred in extrastriate cortex (middle occipital gyrus, BA 19) but not in the primary visual cortex. Later attention-related reactivations in the primary visual cortex were found at about 110 ms after stimulus onset. The results suggest that involuntary as well as voluntary attention modulates visual processing at the level of extrastriate cortex; however, at least some different processes are involved by involuntary attention compared to voluntary attention. In addition, the possible feedback from higher visual cortex to the primary visual cortex is faster and occurs earlier in involuntary relative to voluntary attention task.

Figure 1

Schematic illustration of the procedure of the present study. Each cue consisted of four small dots in the corner of a virtual square and was presented for 50 ms prior to the stimuli. Each stimulus consisted of two horizontal, one vertical, and one diagonal line and was presented for 100 ms. Cue‐to‐stimulus SOA was fixed at 150 ms. The cue predicted the location of the stimulus in 50% of trials. Participants' task was to respond to the orientation of the only diagonal line in the stimulus display (“/” vs. “\”). 20% of trials are cue‐only trials without presentation of the stimulus array.

Figure 2

a: Grand average ERPs across 12 participants for valid and invalid cue‐plus‐stimulus trials when the stimuli appeared in the LVF. Note that time zero is the onset of the cues, with the onset of the stimuli (marked by an arrow) 150 ms after cue onset. The ERP to the stimulus was overlapped by the ERP to the cue because of fixed and short cue‐to‐stimulus SOA. b: The ERPs for LVF‐cue‐plus‐LVF‐stimulus trials and LVF‐cue‐only trials. The difference waves obtained by subtracting the ERPs of left‐cue‐only trials from ERPs of left‐cue‐plus‐left‐stimulus trials were the ERPs of valid stimuli in LVF. Similar subtraction procedure was applied to obtain ERPs of invalid trials in LVF, and valid and invalid trials in RVF. See text for details of the subtraction procedure.

Figure 3

The ERPs of valid and invalid stimuli in LVF (a) and RVF (b) after ERP subtraction. Time zero is the onsets of the cues, and 150 ms is the onsets of the stimuli (marked by an arrow). Attentional modulation on the P1 and N1 components was consistently observed at posterior sites (P3/P4, OL/OR, T5/T6) contralateral to stimulus side.

Figure 4

The mean amplitude and latency of the contralateral P1 and N1 components for valid and invalid trials at posterior sites (P3/P4, T5/T6, and OL/OR). Data were averaged across visual field and hemisphere. Valid trials elicited a larger and later contralateral P1, and a smaller and later contralateral N1 than invalid trials.

Figure 5

The LORETA localization of the C1 component in response to valid and invalid stimulus in LVF (a) and RVF (b). The activations were compared between valid and invalid trials at the location where strongest activation was found for valid trials. Activation in primary visual cortex (around the calcarine fissure, marked by black circles) was observed in the sagittal view of the brain, and the activation strength was comparable between valid and invalid stimuli for both LVF and RVF stimulus.

Figure 6

a: The attention‐related waves obtained by subtracting ERPs of invalid trials from ERPs of valid trials in LVF (left column) and RVF (right column). Time zero is the onset of the cue, and 150 ms is the onset of the stimuli. There was a positive going component which peaked at about 140 ms (P140) on the posterior side contralateral to stimulus location. This contralateral distribution of P140 is shown on the scalp voltage distribution maps aside the difference waveforms (color scale, –5 to 5 μV for both LVF and RVF stimuli). b: The strongest attention‐related activation found by LORETA for LVF and RVF stimuli. c: Surface view of the attention‐related brain activations for LVF and RVF stimuli. See Table I for the brain areas activated by visuospatial attention. ERP data were averaged from 106 to 166 ms for (b) and (c).

Figure 7

Time course of the attention‐related brain activations from 102 ms to 124 ms every 8 ms when the stimulus appeared in LVF (a) and RVF (b). Activations in the contralateral middle occipital/temporal area (47, –67, 15, BA 19 for LVF stimuli; and –52, –68, 8, BA 19/39 for RVF stimuli) were observed at 124 ms after stimulus onset. Activations in the primary visual cortex (–10, –95, –13, BA 17) were observed at 102 ms (LVF) and 110 ms (RVF) after stimulus onset, along with activations in other visual cortex.