A Retinotopic Basis for the Division of High-Level Scene Processing between Lateral and Ventral Human Occipitotemporal Cortex.
TL;DR: It is demonstrated that scene-selective regions exhibit strong biases for different portions of the visual field, with the lateral region representing the contralateral lower visual field and the ventral region the contralsateral upper visual field.
Abstract: In humans, there is a repeated category-selective organization across the lateral and ventral surfaces of the occipitotemporal cortex. This apparent redundancy is often explained as a feedforward hierarchy, with processing within lateral areas preceding the processing within ventral areas. Here, we tested the alternative hypothesis that this structure better reflects distinct high-level representations of the upper (ventral surface) and lower (lateral surface) contralateral quadrants of the visual field, consistent with anatomical projections from early visual areas to these surfaces in monkey. Using complex natural scenes, we provide converging evidence from three independent functional imaging and behavioral studies. First, population receptive field mapping revealed strong biases for the contralateral upper and lower quadrant within the ventral and lateral scene-selective regions, respectively. Second, these same biases were observed in the position information available both in the magnitude and multivoxel response across these areas. Third, behavioral judgments of a scene property strongly represented within the ventral scene-selective area (open/closed), but not another equally salient property (manmade/natural), were more accurate in the upper than the lower field. Such differential representation of visual space poses a substantial challenge to the idea of a strictly hierarchical organization between lateral and ventral scene-selective regions. Moreover, such retinotopic biases seem to extend beyond these regions throughout both surfaces. Thus, the large-scale organization of high-level extrastriate cortex likely reflects the need for both specialized representations of particular categories and constraints from the structure of early vision.
SIGNIFICANCE STATEMENT One of the most striking findings in fMRI has been the presence of matched category-selective regions on the lateral and ventral surfaces of human occipitotemporal cortex. Here, we focus on scene-selective regions and provide converging evidence for a retinotopic explanation of this organization. Specifically, we demonstrate that scene-selective regions exhibit strong biases for different portions of the visual field, with the lateral region representing the contralateral lower visual field and the ventral region the contralateral upper visual field. These biases are consistent with the retinotopy found in the early visual areas that lie directly antecedent to category-selective areas on both surfaces. Furthermore, these biases extend beyond scene-selective cortex and provide a retinotopic basis for the large-scale organization of occipitotemporal cortex.
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TL;DR: It is suggested that this problem can be resolved by questioning the utility of the classical low- to high-level framework of visual perception for scene processing, and why low- and mid-level properties may be particularly diagnostic for the behavioural goals specific to scene perception as compared to object recognition.
Abstract: Visual scene analysis in humans has been characterized by the presence of regions in extrastriate cortex that are selectively responsive to scenes compared with objects or faces. While these regions have often been interpreted as representing high-level properties of scenes (e.g. category), they also exhibit substantial sensitivity to low-level (e.g. spatial frequency) and mid-level (e.g. spatial layout) properties, and it is unclear how these disparate findings can be united in a single framework. In this opinion piece, we suggest that this problem can be resolved by questioning the utility of the classical low- to high-level framework of visual perception for scene processing, and discuss why low- and mid-level properties may be particularly diagnostic for the behavioural goals specific to scene perception as compared to object recognition. In particular, we highlight the contributions of low-level vision to scene representation by reviewing (i) retinotopic biases and receptive field properties of scene-selective regions and (ii) the temporal dynamics of scene perception that demonstrate overlap of low- and mid-level feature representations with those of scene category. We discuss the relevance of these findings for scene perception and suggest a more expansive framework for visual scene analysis.This article is part of the themed issue 'Auditory and visual scene analysis'.
162 citations
16 Sep 2019
TL;DR: Challenges for the future include developing computational models of information processing in scene regions, investigating how these regions support scene perception under ecologically realistic conditions, and understanding how they operate in the context of larger brain networks.
Abstract: Humans are remarkably adept at perceiving and understanding complex real-world scenes. Uncovering the neural basis of this ability is an important goal of vision science. Neuroimaging studies have identified three cortical regions that respond selectively to scenes: parahippocampal place area, retrosplenial complex/medial place area, and occipital place area. Here, we review what is known about the visual and functional properties of these brain areas. Scene-selective regions exhibit retinotopic properties and sensitivity to low-level visual features that are characteristic of scenes. They also mediate higher-level representations of layout, objects, and surface properties that allow individual scenes to be recognized and their spatial structure ascertained. Challenges for the future include developing computational models of information processing in scene regions, investigating how these regions support scene perception under ecologically realistic conditions, and understanding how they operate in the context of larger brain networks.
158 citations
17 Sep 2018
TL;DR: An organizational scheme that marries form and function and provides a framework for future research is described, which invokes an innately determined organization refined by visual experience that is consistent with principles of cortical development and principles of evolution.
Abstract: Inferior temporal cortex (IT) is a key part of the ventral visual pathway implicated in object, face, and scene perception. But how does IT work? Here, I describe an organizational scheme that marries form and function and provides a framework for future research. The scheme consists of a series of stages arranged along the posterior-anterior axis of IT, defined by anatomical connections and functional responses. Each stage comprises a complement of subregions that have a systematic spatial relationship. The organization of each stage is governed by an eccentricity template, and corresponding eccentricity representations across stages are interconnected. Foveal representations take on a role in high-acuity object vision (including face recognition); intermediate representations compute other aspects of object vision such as behavioral valence (using color and surface cues); and peripheral representations encode information about scenes. This multistage, parallel-processing model invokes an innately determined organization refined by visual experience that is consistent with principles of cortical development. The model is also consistent with principles of evolution, which suggest that visual cortex expanded through replication of retinotopic areas. Finally, the model predicts that the most extensively studied network within IT-the face patches-is not unique but rather one manifestation of a canonical set of operations that reveal general principles of how IT works.
143 citations
Cites background from "A Retinotopic Basis for the Divisio..."
...The idea that the functional organization of extrastriate visual cortex is determined by retinotopic principles of V1 as they relate to behavior has been extended to consider asymmetries in upper and lower visual fields (Groen et al. 2017, Silson et al. 2015)....
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TL;DR: It is shown that a specific region in the human visual system, known as the occipital place area, automatically encodes the structure of navigable space in visual scenes, thus providing evidence for a bottom-up visual mechanism for perceiving potential paths for movement in one’s immediate surroundings.
Abstract: A central component of spatial navigation is determining where one can and cannot go in the immediate environment. We used fMRI to test the hypothesis that the human visual system solves this problem by automatically identifying the navigational affordances of the local scene. Multivoxel pattern analyses showed that a scene-selective region of dorsal occipitoparietal cortex, known as the occipital place area, represents pathways for movement in scenes in a manner that is tolerant to variability in other visual features. These effects were found in two experiments: One using tightly controlled artificial environments as stimuli, the other using a diverse set of complex, natural scenes. A reconstruction analysis demonstrated that the population codes of the occipital place area could be used to predict the affordances of novel scenes. Taken together, these results reveal a previously unknown mechanism for perceiving the affordance structure of navigable space.
128 citations
Cites background from "A Retinotopic Basis for the Divisio..."
...Furthermore, the OPA is known to show a retinotopic bias for information in the periphery, which could facilitate the perception of extended spatial structures, and also a bias for the lower visual field, where paths tend to be (31)....
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TL;DR: It is argued that for a complete view of scene understanding, it is necessary to account for both differing observer goals and the contribution of diverse scene properties.
119 citations
References
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TL;DR: A model for the organization of this system that emphasizes a distinction between the representation of invariant and changeable aspects of faces is proposed and is hierarchical insofar as it is divided into a core system and an extended system.
4,430 citations
"A Retinotopic Basis for the Divisio..." refers background in this paper
...This duplicate organization is often interpreted within a hierarchical framework (Haxby et al., 2000) wherein lateral areas correspond to early and ventral areas to later processing stages (Grill-Spector et al....
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...This duplicate organization is often interpreted within a hierarchical framework (Haxby et al., 2000) wherein lateral areas correspond to early and ventral areas to later processing stages (Grill-Spector et al., 1999; Kourtzi and Kanwisher, 2001; Lerner et al., 2001; Kourtzi et al., 2003; Downing…...
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TL;DR: Evidence is presented that a particular area within human parahippocampal cortex is involved in a critical component of navigation: perceiving the local visual environment, and it is proposed that the PPA represents places by encoding the geometry of the local environment.
Abstract: Medial temporal brain regions such as the hippocampal formation and parahippocampal cortex have been generally implicated in navigation and visual memory. However, the specific function of each of these regions is not yet clear. Here we present evidence that a particular area within human parahippocampal cortex is involved in a critical component of navigation: perceiving the local visual environment. This region, which we name the 'parahippocampal place area' (PPA), responds selectively and automatically in functional magnetic resonance imaging (fMRI) to passively viewed scenes, but only weakly to single objects and not at all to faces. The critical factor for this activation appears to be the presence in the stimulus of information about the layout of local space. The response in the PPA to scenes with spatial layout but no discrete objects (empty rooms) is as strong as the response to complex meaningful scenes containing multiple objects (the same rooms furnished) and over twice as strong as the response to arrays of multiple objects without three-dimensional spatial context (the furniture from these rooms on a blank background). This response is reduced if the surfaces in the scene are rearranged so that they no longer define a coherent space. We propose that the PPA represents places by encoding the geometry of the local environment.
2,842 citations
"A Retinotopic Basis for the Divisio..." refers background or methods in this paper
...We used three independent approaches to investigate retinotopic biases in scene-selective transverse occipital sulcus (TOS; or occipital place area; Dilks et al., 2013) on the lateral surface and in parahippocampal place area (PPA; Epstein and Kanwisher, 1998) on the ventral surface....
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..., 2013) on the lateral surface and in parahippocampal place area (PPA; Epstein and Kanwisher, 1998) on the ventral surface....
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TL;DR: Cortical magnification factor curves for striate and extrastriate cortical areas were determined, which showed that human visual areas have a greater emphasis on the center-of-gaze than their counterparts in monkeys.
Abstract: The borders of human visual areas V1, V2, VP, V3, and V4 were precisely and noninvasively determined. Functional magnetic resonance images were recorded during phase-encoded retinal stimulation. This volume data set was then sampled with a cortical surface reconstruction, making it possible to calculate the local visual field sign (mirror image versus non-mirror image representation). This method automatically and objectively outlines area borders because adjacent areas often have the opposite field sign. Cortical magnification factor curves for striate and extrastriate cortical areas were determined, which showed that human visual areas have a greater emphasis on the center-of-gaze than their counterparts in monkeys. Retinotopically organized visual areas in humans extend anteriorly to overlap several areas previously shown to be activated by written words.
2,590 citations
TL;DR: The lateral occipital complex (LO) showed preferential activation to images of objects, compared to a wide range of texture patterns as mentioned in this paper, suggesting that objects varying widely in their recognizability (e.g., famous faces, common objects, and unfamiliar three-dimensional abstract sculptures) activated it to a similar degree.
Abstract: The stages of integration leading from local feature analysis to object recognition were explored in human visual cortex by using the technique of functional magnetic resonance imaging. Here we report evidence for object-related activation. Such activation was located at the lateral-posterior aspect of the occipital lobe, just abutting the posterior aspect of the motion-sensitive area MT/V5, in a region termed the lateral occipital complex (LO). LO showed preferential activation to images of objects, compared to a wide range of texture patterns. This activation was not caused by a global difference in the Fourier spatial frequency content of objects versus texture images, since object images produced enhanced LO activation compared to textures matched in power spectra but randomized in phase. The preferential activation to objects also could not be explained by different patterns of eye movements: similar levels of activation were observed when subjects fixated on the objects and when they scanned the objects with their eyes. Additional manipulations such as spatial frequency filtering and a 4-fold change in visual size did not affect LO activation. These results suggest that the enhanced responses to objects were not a manifestation of low-level visual processing. A striking demonstration that activity in LO is uniquely correlated to object detectability was produced by the "Lincoln" illusion, in which blurring of objects digitized into large blocks paradoxically increases their recognizability. Such blurring led to significant enhancement of LO activation. Despite the preferential activation to objects, LO did not seem to be involved in the final, "semantic," stages of the recognition process. Thus, objects varying widely in their recognizability (e.g., famous faces, common objects, and unfamiliar three-dimensional abstract sculptures) activated it to a similar degree. These results are thus evidence for an intermediate link in the chain of processing stages leading to object recognition in human visual cortex.
1,697 citations
TL;DR: This work identified the borders between several retinotopically organized visual areas in the posterior occipital lobe and estimated the spatial resolution of the fMRI signal and found that signal amplitude falls to 60% at a spatial frequency of 1 cycle per 9 mm of visual cortex.
Abstract: A method of using functional magnetic resonance imaging (fMRI) to measure retinotopic organization within human cortex is described. The method is based on a visual stimulus that creates a traveling wave of neural activity within retinotopically organized visual areas. We measured the fMRI signal caused by this stimulus in visual cortex and represented the results on images of the flattened cortical sheet. We used the method to locate visual areas and to evaluate the spatial precision of fMRI. Specifically, we: (i) identified the borders between several retinotopically organized visual areas in the posterior occipital lobe; (ii) measured the function relating cortical position to visual field eccentricity within area V1; (iii) localized activity to within 1.1 mm of visual cortex; and (iv) estimated the spatial resolution of the fMRI signal and found that signal amplitude falls to 60% at a spatial frequency of 1 cycle per 9 mm of visual cortex. This spatial resolution is consistent with a linespread whose full width at half maximum spreads across 3.5 mm of visual cortex. In a series of experiments, we measured the retinotopic organization of human cortical area V1 and identified the locations of other nearby retinotopically organized visual areas. We also used the retinotopic organization of human primary visual cortex to measure the spatial localization and spatial resolution that can be obtained from functional magnetic resonance imaging (fMRI) of human visual cortex. Human primary visual cortex (area V1) is located in the
1,585 citations
"A Retinotopic Basis for the Divisio..." refers background in this paper
...In human, representations of the lower and upper fields are similarly segregated in early visual areas (Sereno et al., 1995; DeYoe et al., 1996; Engel et al., 1997), which lie directly antecedent to category-selective regions on both surfaces....
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