Attentional selection of multiple objects in the human visual system

Abstract

Classic theories of object-based attention assume a single object of selection but real-world tasks, such as driving a car, often require attending to multiple objects simultaneously. However, whether object-based attention can operate on more than one object at a time remains unexplored. Here, we used functional magnetic resonance imaging (fMRI) to address this question as human participants performed object-based attention tasks that required simultaneous attention to two objects differing in either their features or locations. Simultaneous attention to two objects differing in features (face and house) did not show significantly different responses in the fusiform face area (FFA) or parahippocampal place area (PPA), respectively, compared to attending a single object (face or house), but did enhance the response in the inferior frontal gyrus (IFG). Simultaneous attention to two circular arcs differing in locations did not show significantly different responses in the primary visual cortex (V1) compared to attending a single circular arc, but did enhance the response in the intraparietal sulcus (IPS). These results suggest that object-based attention can simultaneously select at least two objects differing in their features or locations, processes mediated by the frontal and parietal cortex, respectively.

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: Fusiform face area; Inferior frontal gyrus; Intraparietal sulcus; Object-based attention; Parahippocampal place area; fMRI.

Conflict of interest statement

Conflict of interest

The authors declare no competing financial interests.

Published by Elsevier Inc.

Figures

Fig. 1

A sample stimulus and two hypotheses of Experiment 1. A A sample stimulus of a superimposed face and a house, with the face and house displaced (i.e., a face static with a house static condition, SFSH) to the right of fixation (about 1.0° eccentricity) as required for the static position-repetition detection task. B Two hypotheses of Experiment 1. Single-object attention (top): The attended feature (the motion direction or static position) in two objects (face and house) versus in a single object (face or house) should show reduced responses in FFA and PPA, respectively. Two-object attention (bottom): The attended feature in two objects (face and house) versus in a single object (face or house) should not show significantly different responses in FFA and PPA, respectively.

Fig. 2

Results of Experiment 1. A Face-, house-, and motion-selective areas depicted on the brain of a single subject. The ROI in FFA was defined as an area that responded more strongly to faces than houses. The ROI in PPA was defined as an area that responded more strongly to houses than faces. The ROI in MT+ was defined as an area that responded more strongly to the moving stimuli than static stimuli. B Event-related BOLD signals and their peak amplitudes of ROIs in FFA (top), PPA (middle), and MT+ (bottom) during the Attend Moving scan. C Event-related BOLD signals and their peak amplitudes of ROIs in FFA (top), PPA (middle), and MT+ (bottom) during the Attend Static scan. D Object-based attention effect of the single-object and two-object conditions in FFA and PPA during the Attend Moving scans. Compared to the SFMH condition, enhanced responses in the MFSH and MFMH conditions indicated the object-based attention effect in FFA for the single-object and two-object conditions, respectively; compared to the MFSH condition, enhanced responses in the SFMH and MFMH conditions indicated an object-based attention effect in PPA for the single-object and two-object conditions, respectively. E Object-based attention effect of the single-object and two-object conditions in FFA and PPA during the Attend Static scans. Compared to the MFSH condition, the enhanced response in the SFMH and SFSH conditions indicated an object-based attention effect in FFA for the single-object and two-object conditions, respectively; compared to the SFMH condition, enhanced responses in the MFSH and SFSH conditions indicated an object-based attentional effect in PPA for the single-object and two-object conditions, respectively. Error bars denote 1 SEM calculated across sixteen participants.

Fig. 3

Stimuli and design of Experiment 2. A Stimuli and conditions. The stimulus display contained three circular arcs, two of which were presented in the same visual field (in this case, in the right visual field). Single cue: an empty wedge overlapped one end of a circular arc; double cue: two single cues, diametrically opposite to each other, overlapped the ends of two different circular arcs. The target appeared frequently (75% of the trials) at the pre-cued location (Valid Cue, VC). It could also appear either at the uncued end of the pre-cued circular arc (Invalid Cue Same Object, ICSO, 12.5% of the trials), or at the equidistant end of the uncued circular arc (Invalid Cue Different Object, ICDO, 12.5% of the trials). B Double cue same hemifield. Two cues were presented in the same visual field. C Double cue opposite hemifields. Two cues were presented in the opposite visual field. D ROI definition. Checkered wedges were used to define ROIs in human V1. E fMRI protocol. The fixation cross was presented for 8, 10, or 12 s, followed by the single cue or the double cue presented for 6, 8, or 10 s. Then a target was presented for 120 ms at one end of a circular arc. Participants pressed one of two buttons as rapidly and correctly as possible to indicate the color of the target (red or green).

Fig. 4

Results of Experiment 2. A ROIs in V1 were defined as retinotopic loci corresponding to the six ends of the three circular arcs. B Mean RTs are shown for VC, ICSO, and ICDO in the single (left) and double (right) cue conditions. C Object-based attention effect (left) and spatial attention effect (right) of the single and double cue conditions for RTs. D BOLD amplitude of ROIs in V1 evoked by VC, ICSO, and ICDO in the single (left) and double (right) cue conditions during cueing phase. E Object-based attention effect (left) and spatial attention effect (right) of the single and double cue conditions during the cueing phase. F BOLD amplitude of ROIs in V1 evoked by the target for VC, ICSO, and ICDO in the single (left) and double (right) cue conditions. G Object-based attention effect (left) and spatial attention effect (right) of the single and double cue conditions during the target phase. H BOLD amplitude of ROIs in V1 evoked by ICSO and ICDO in the single (left) and double (right) cue conditions during the target phase. I Object-based attention effect of the single and double cue conditions for the valid and invalid target conditions. Error bars denote 1 SEM calculated across sixteen participants.

Fig. 5

Results of a whole brain analysis. A Experiment 1: The inferior frontal gyrus (IFG, talairach coordinates: Left: −45 ± 1.01, 27 ± 1.78, 13 ± 1.52; Right: 41 ±1.34, 19 ± 1.94, 14 ± 1.27, p < 0.01 with FDR correction) showed a greater response in the two-object condition than the single-object condition in both the Attend Moving (top) and Attend Static (bottom) scans, and their BOLD signal amplitudes. B Correlations between the enhanced IFG response in the two-object condition relative to the single-object condition and the COBAE in FFA (left) and PPA (right). COBAE = OBAE Single-object – OBAE Two-object, where OBAE Single-object and OBAE Two-object are the object-based attention effect in the single-object and two-object conditions, respectively. C Experiment 2: The intraparietal sulcus (IPS, talairach coordinates: Left: −20 ± 1.22, −88 ± 1.56, 25 ± 1.48; Right: 27 ±1.16, −83 ± 1.49, 27 ± 1.39, p < 0.01 with FDR correction) showed a greater response in the two-object condition than the single-object condition, and its BOLD signal amplitudes. EVC: early visual cortex. D Correlations between the enhanced IPS response in the two-object condition relative to the single-object condition and CSAE (left), and COBAE (right). CSAE = SAE Single-object – SAE Two-object, where SAE Single-object and SAE Two-object are the spatial attention effect in the single-object and two-object conditions, respectively. Error bars denote 1 SEM calculated across sixteen participants.