Not one extrastriate body area: Using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex
Research highlights
► Not one EBA: 3 limb-selective clusters in a crescent organization surrounding hMT+. ► Each limb-selective cluster has a distinct anatomical location. ► LO and TO visual field maps verify parcellation of LOTC limb-selective activations. ► Different position and body part selectivity among LOTC limb-selective activations. ► New multi-factor criteria for parcellating high-level visual cortex using fMRI.
Introduction
Neuroimaging studies in the field of high level vision have identified an activation in human lateral occipitotemporal cortex (LOTC) known as the extrastriate body area (EBA) that is selective for images of the body and body parts relative to a variety of control images (Downing et al., 2001, Orlov et al., 2010, Peelen and Downing, 2007a, Pinsk et al., 2009, Schwarzlose et al., 2008, Spiridon et al., 2006). Though this activation is typically localized by contrasting neural responses to images of headless bodies and body parts (most often limbs, such as arms and legs), relative to objects, faces, and places, there is considerable variability in the types of images and statistical contrasts used to localize the EBA (Supplemental Table 1). Additionally, there is a lack of anatomical and functional specificity in the boundaries demarcating the EBA. Researchers loosely identify the EBA as a large swath of cortex extending from the lateral occipital sulcus (LOS) to portions of the inferotemporal gyrus (ITG), often encompassing the ascending limb of the posterior inferotemporal sulcus (pITS; Peelen and Downing, 2007a, Peelen et al., 2006). However, the pITS is also the location of an extensively studied region involved in motion perception, the human MT+ complex (hMT+; DeYoe et al., 1996, Dumoulin et al., 2000, Huk et al., 2002, Tootell et al., 1995). Even though the EBA and hMT+ are accepted to be cortical neighbors on the pITS (Downing et al., 2007), no group has examined their spatial relationship with high-resolution fMRI, leaving open the question: What is the fine-scale spatial organization among body part- and motion-selective voxels in LOTC?
The prevailing view in the field is that the EBA is a distinct visual area based on its body part selectivity (Downing et al., 2001, Kanwisher, 2010, Op de Beeck et al., 2008, Peelen and Downing, 2007a) and that it substantially overlaps hMT+ on the pITS (Downing et al., 2007, Peelen and Downing, 2007a). This suggests an organization where these two regions share a large extent of cortex with the EBA located posterior to and overlapping with hMT+ (Fig. 1a; based on descriptions by Peelen and Downing, 2007a, Peelen et al., 2006). However, when using un-segmented brain volume visualizations, it is complicated to get an accurate understanding of the spatial relationship between these LOTC activations because the apparent organization is dependent on the viewing axis. For example, in Fig. 2 of Downing et al., 2007, the EBA appears to be posterior and superior to hMT+ on the sagittal view, but on the axial view, the EBA extends anterior to hMT+ onto the middle temporal gyrus (MTG). Indeed, with improved visualizations on the inflated cortical surface rather than on the un-segmented brain volume, the EBA does not appear as a single spherical activation posterior to hMT+ (see Figs. 2 and 3 from Spiridon et al., 2006; Supplemental Fig. 3 from Schwarzlose et al., 2008). Instead, the EBA seems to surround hMT+. A common feature we infer from these cortical surface visualizations is an organization containing body part-selective voxels in a ring-like structure sparing a central, non-overlapping portion of hMT+ (Fig. 1b). Though this ring structure has been illustrated also in EBA studies that have not included hMT+ (Fig. 6 from Pinsk et al., 2009; Fig. 2 from Orlov et al., 2010), this ring organization has never been referenced or examined in prior studies.
While at first glance, it may not seem crucial if the EBA is arranged either as a spherical cluster or a ring (as long as it contiguous), a contiguous activation does not indicate homogeneity at either the voxel or neural level. An analogous ring organization exists in early visual cortex where eccentricity bands span a contiguous set of voxels surrounding the confluent fovea. However, researchers do not average data across an entire eccentricity band because it is well known that receptive field properties across an eccentricity band differ across adjacent visual areas and their properties become more differentiated as the cortical distance between areas increases (Boussaoud et al., 1991, Dumoulin and Wandell, 2008, Grill-Spector and Malach, 2004). Thus, in fMRI studies, continuous eccentricity bands are divided into distinct visual areas using a separate polar angle measurement. Consequently, even if the EBA is observed as a continuous ring of activation, it raises two questions: (1) Is the EBA a homogeneous cortical region, or does it include separate heterogeneous activations? (2) What criteria should be used to divide this activation?
Classic neuroscience studies use several independent criteria to guide the decision of parcellating cortical regions into distinct areas (Desimone and Ungerleider, 1986, Felleman and Van Essen, 1991 are two such examples). These criteria include anatomical location, cytoarchitecture, connectivity, topographic organization, and function. Though we cannot use all of these criteria when noninvasively measuring functional activations in humans with fMRI, we can directly measure anatomical location, topographic organization, and function, as well as use knowledge from prior studies examining cytoarchitecture and connectivity to support or refute further parcellation.
One way to apply these methods to the current research is to examine the relation between body part-selective activations and the region they neighbor: hMT+. In humans, hMT+ is identified based on its motion selectivity and location in the pITS (Dumoulin et al., 2000). Examining the relation between the body part-selective activations and hMT+ is particularly appealing because the posterior component of the hMT+ complex, area MT (also referred to as V5; Watson et al., 1993, Zeki et al., 1991), is one of only a handful of brain areas widely accepted to exist across primates (Kaas, 2005, Zeki, 2004). Anatomical studies of postmortem human brains indicate that area MT is a distinct ovoid region that is densely myelinated. The cortex surrounding MT is crescent-shaped, has a different cytoarchitecture, is less myelinated, and understood to be a region separate from MT known as MT crescent (MTc; Tootell and Taylor, 1995). Moreover, anatomical studies in both old and new world monkeys document a similar MTc region that is distinct from MT (owl monkeys: Kaas and Morel, 1993, Tootell et al., 1985; green monkeys and macaques: Tootell and Taylor, 1995). In macaques, MTc has been further separated into areas V4t and FST based on differences in motion and position sensitivity, as well as cortico-cortical connections (Desimone and Ungerleider, 1986, Felleman and Van Essen, 1991). Thus, in both humans and monkeys, the underlying cytoarchitecture within MT is different than its immediate surround, where MTc has been identified as a single area by some researchers or several distinct areas by others. This divided crescent suggests a third possible organization of LOTC (Fig. 1c) where several limb-selective activations surround hMT+ based on their anatomical location and potential underlying differences in cytoarchitecture and function.
Another source of information for deciding whether to split or to combine functional activations in visual cortex is the finding that visual field maps consistently co-localize with specific anatomical landmarks. MT, for example, contains a hemifield map starting from the lower vertical meridian in the pITS ending with the upper vertical meridian more anteriorly. Eccentricity is organized such that the foveal representation is located on the inferior portion of the pITS and the peripheral representation extends to the superior portion of the pITS (Huk et al., 2002). This relationship between anatomical location and visual field maps is prevalent in early visual cortex and throughout LOTC (Wandell et al., 2007). It is possible that the body part-selective activations potentially surrounding hMT+ (1) can be reliably dissociated based on anatomical location and (2) that this parcellation can be verified by visual field maps. Further, improved imaging of LOTC with high-resolution fMRI will reduce partial voluming effects, address overlap effects, and aid in defining this portion of cortex more accurately. We recently used these methods in ventral temporal cortex, discovering a consistent topography of face- and limb-selective activations both relative to each other as well as to known visual field maps on the fusiform gyrus and occipitotemporal sulcus (Weiner and Grill-Spector, 2010).
In the present study, we examined the spatial organization of the EBA relative to hMT+ and known LOTC visual field maps at a finer spatial scale in order to address the following questions:
- (1)
Are there separate limb-selective components with distinct anatomical locations surrounding hMT+ (Fig. 1)?
- (2)
Does the location of LOTC visual field maps support or refute the parcellation of limb-selective activations based on anatomical location?
- (3)
If LOTC limb-selective activations can be reliably parcellated, can they be functionally dissociated based on their category selectivity and position sensitivity?
Section snippets
Subjects
Nine subjects (3 females, ages 24–39) participated in three experiments: six category experiment (sessions one and two), motion experiment (sessions one and two), and visual field mapping (session three). Six of these subjects also participated in an experiment during which we measured responses to limbs across three positions in the visual field (session four). A subset of these subjects also participated in additional sessions of control mapping experiments used to parcellate hMT+ into MT and
Three limb-selective activations with distinct anatomical locations surrounding hMT+
Using high-resolution fMRI measurements, we first examined the spatial organization of limb-selective and motion-selective responses in LOTC relative to each other in order to test the three scenarios proposed in Fig. 1. The first scenario (Fig. 1a) is the standard model describing the spatial relationship between the EBA and hMT+, according to which there is one contiguous spherical EBA located posterior (and a bit superior) to, as well as largely overlapping with, hMT+ on the posterior
Discussion
The current study examines the fine-scale spatial organization of limb- and motion-selective responses in lateral occipitotemporal cortex (LOTC), and reports three separate limb-selective activations organized in a crescent surrounding the human MT+ complex (hMT+), rather than one contiguous extrastriate body area (EBA) overlapping hMT+, supporting the organization in Fig. 1c. Each limb-selective activation is located relative to distinct anatomical landmarks corresponding to separate portions
Acknowledgments
This work was supported by National Eye Institute 1R21EY017741; NSF BCS 0617688, NSF BCS 0920865, and Whitehall Foundation 2005-05-111-RES grants to KGS. We thank Rory Sayres for helping with the data collection, Jon Winawer, and Nathan Witthoft for comments on the manuscript, as well as Anthony Wagner and Brian Wandell for the useful conversations. We thank Paul Downing, Marius Peelen, Tanya Orlov, and Udi Zohary for headless body and body part stimuli to directly compare our data to their
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