Behaviorally Relevant Abstract Object Identity Representation in the Human Parietal Cortex

Abstract

The representation of object identity is fundamental to human vision. Using fMRI and multivoxel pattern analysis, here we report the representation of highly abstract object identity information in human parietal cortex. Specifically, in superior intraparietal sulcus (IPS), a region previously shown to track visual short-term memory capacity, we found object identity representations for famous faces varying freely in viewpoint, hairstyle, facial expression, and age; and for well known cars embedded in different scenes, and shown from different viewpoints and sizes. Critically, these parietal identity representations were behaviorally relevant as they closely tracked the perceived face-identity similarity obtained in a behavioral task. Meanwhile, the task-activated regions in prefrontal and parietal cortices (excluding superior IPS) did not exhibit such abstract object identity representations. Unlike previous studies, we also failed to observe identity representations in posterior ventral and lateral visual object-processing regions, likely due to the greater amount of identity abstraction demanded by our stimulus manipulation here. Our MRI slice coverage precluded us from examining identity representation in anterior temporal lobe, a likely region for the computing of identity information in the ventral region. Overall, we show that human parietal cortex, part of the dorsal visual processing pathway, is capable of holding abstract and complex visual representations that are behaviorally relevant. These results argue against a "content-poor" view of the role of parietal cortex in attention. Instead, the human parietal cortex seems to be "content rich" and capable of directly participating in goal-driven visual information representation in the brain.

Significance statement: The representation of object identity (including faces) is fundamental to human vision and shapes how we interact with the world. Although object representation has traditionally been associated with human occipital and temporal cortices, here we show, by measuring fMRI response patterns, that a region in the human parietal cortex can robustly represent task-relevant object identities. These representations are invariant to changes in a host of visual features, such as viewpoint, and reflect an abstract level of representation that has not previously been reported in the human parietal cortex. Critically, these neural representations are behaviorally relevant as they closely track the perceived object identities. Human parietal cortex thus participates in the moment-to-moment goal-directed visual information representation in the brain.

Keywords: attention; fMRI MVPA; face perception; parietal cortex; visual representation.

Figure 1.

Experiment 1 stimuli, trial structure, and ROIs. A, Example images from a block of face trials. Face images from two well known actors, Leonardo DiCaprio and Matt Damon, were used. Within a block of trials, observers viewed a sequential presentation of 10 face images sharing the same identity but differed in viewpoint, hairstyle, facial expression, and age. Observers were asked to detect the occasional presence of an oddball face chosen from one of eight other actors. James Dean's face is shown here as the oddball face among Leonardo DiCaprio's faces. B, Example images from a block of name trials. Actor names were written in different fonts, and observers were again asked to detect an oddball. James Dean's name is shown here as the oddball name among Leonardo DiCaprio's names. An oddball occurred rarely, and blocks containing the oddball were removed from further analyses. C, Example ROIs from one representative observer.

Figure 2.

Experiment 1 design and results. A, Schematic illustration of the key comparisons made in the experiment. To evaluate the existence of abstract face-identity representation in each ROI, we examined whether the within-identity correlation was greater than the between-identity correlation. The within-identity correlation referred to the correlation of the fMRI voxel response patterns between two face sets (or two name sets) from the same actor, whereas the between-identity correlation referred to the pattern correlation between two face sets (or two name sets), each from a different actor. B, Fisher-transformed correlation coefficients (z) between the face sets in superior IPS, LO region, the right FFA, and VWFA ROIs. Only superior IPS showed a higher within-identity than between-identity correlation, indicating the presence of abstract face-identity representation in this brain region despite large variations in viewpoint, hairstyle, facial expression, and age of the face images used. C, Fisher-transformed correlation coefficients between the name sets in the same brain regions. None of the regions showed a higher within-identity than between-identity correlation, indicating the absence of identity representation in these brain regions when name stimuli were used. Gray and white bars indicate within-identity and between-identity correlations, respectively. Error bars indicate the within-subject SEMs. *p < 0.05.

Figure 3.

Experiment 2 design and results. A, Schematic illustration of the key comparisons made in the experiment. Similar to the faces and the names in Experiment 1, we examined whether the within-identity correlations were greater than the between-identity correlations for car images and car names. B, Fisher-transformed correlation coefficients (z) between the car image sets in superior IPS, LO region, PPA, and VWFA ROIs. Replicating the results for faces in Experiment 1, only superior IPS showed a higher within-identity than between-identity correlation for car images, indicating the presence of abstract car identity representation in this brain region despite large variations in viewpoint, size, and the background scene in which the cars appeared. Note that in both LO and VWFA, the between-identity correlation was greater than the within-identity correlation, possibly reflecting a greater between-set than within-set similarity, which would have worked against the finding of an identity decoding in superior IPS. C, Fisher-transformed correlation coefficients for the car name sets in the same brain regions. As with the face names in Experiment 1, none of the regions showed a higher within-identity than between-identity correlation, indicating the absence of identity representation in these brain regions for the name stimuli. Gray and white bars indicate within-identity and between-identity correlations, respectively. Error bars indicate the within-subject SEMs. *p < 0.05.

Figure 4.

Experiment 3 stimuli and results. A, Example images of the eight actors used. B, Fisher-transformed correlation coefficients (z) between the face image sets in superior IPS, LO region, and the right FFA ROIs. Superior IPS again showed a higher within-identity than between-identity correlation, whereas LO region and the right FFA did not. C, An example face visual search display. Observers performed a speeded visual search for the presence of the face of a target actor among the faces of a distractor actor. A target face appeared in 50% of the trials. In the example shown, Leonardo DiCaprio is the target actor and Russell Crowe is the distractor actor. D, The correlation between the behavioral (as measured by visual search speeds) and the neural (as measured by fMRI pattern correlations) similarity measures of face identity in each ROI. This correlation reached significance only in superior IPS, indicating that the face representations formed there closely tracked the behaviroally perceived face identities. Gray and white bars in B indicate within-identity and between-identity correlations, respectively. Error bars in B indicate the within-subject SEMs. Error bars in D indicate the SDs of the baseline correlation value distributions from the permutation tests (see Materials and Methods). *p < 0.05.

Figure 5.

Comparing representational structures of brain regions using MDS in Experiment 3. The distance between the different brain regions reflected face-identity representation dissimilarity among these regions. A, MDS results for the five ROIs with superior IPS voxels excluded from PPC. Superior IPS was separated from both the ventral visual regions (LO region and the right FFA) and the frontoparietal regions (LPFC and PPC), suggesting that face-identity representation in superior IPS differed from those in the other brain regions. B, MDS results for the five ROIs with both superior IPS and its nearby voxels excluded from PPC. Superior IPS became more separated from PPC in this analysis, showing distinct face-identity representations in these two brain regions. SIPS, Superior IPS.

Figure 6.

The effect of perceptual/image differences on neural response patterns across sets sharing an identity in the three experiments. A, B, Results for face images and face names in Experiment 1. C, D, Results for car images and car names in Experiment 2. E, Results for face images in Experiment 3. While holding the identity constant, the correlation between odd and even runs of the same set was compared with the correlation between two different sets sharing an identity across odd and even runs. A higher within-set than between-set correlation indicates the encoding of the perceptual or image differences between the sets in a brain region. Depending on the experiment and the stimuli used, different ventral object-processing regions showed different amounts of sensitivity to the perceptual/image differences between the sets. Importantly, when identity was held constant, superior IPS never differentiated between sets of images that were identical or different, providing further support that the perceptual/image differences among the sets did not modulate the response pattern in this brain region. Error bars indicate the within-subject SEMs. *p < 0.05.