Efficient object recognition confers an obvious survival advantage and is essential to normal functioning of human everyday life. It is therefore important to study behavioral and neural mechanisms of this essential and complex function. Although single-cell recordings in animals and brain imaging studies in humans have revealed a clear picture of retinotopic mapping in the early visual cortex (Wang, Tanifuji, & Tanaka, 1998
; Engel, Glover, & Wandell, 1997
; Sereno et al., 1995
), it remains uncertain what specific neural correlates are involved and how they are organized functionally for higher levels of object recognition. Some researchers propose that there are functionally encapsulated areas in the ventral processing stream (VPS) specialized for processing different categories of objects or other visual entities (Cohen et al., 2002
; Polk et al., 2002
; Epstein & Kanwisher, 1998
; Kanwisher, McDermott, & Chun, 1997
). Specific stimulus properties that are unique to a particular object category may dictate whether a particular functional region is engaged versus another. Yet others suggest that the underlying principle of functional organization is not based on the type of stimulus or their properties but is driven instead by the perceptual and cognitive demands involved in accessing or differentiating object descriptions (Rogers, Hocking, Mechelli, Patterson, & Price, 2005
; Joseph, 2001
; Gauthier, Tarr, Anderson, Skudlarski, & Gore, 1999
). For example, Rogers et al. (2005)
showed that classifying animals at an intermediate (or basic) level of categorization (e.g., dog or car) activated regions of the fusiform gyrus bilaterally, but classifying vehicles at this intermediate level did not activate these regions. However, when the same objects were classified at a more specific level of categorization (e.g., Labrador or BMW), fusiform activation was observed for both categories of objects. Consequently, these regions of the fusiform gyrus are involved in fine differentiation of object representations rather than being driven by taxonomic category differences or different stimulus properties.
The process of fine differentiation of visually homogenous categories may also explain why the mid-fusiform gyrus is consistently activated for faces compared to some other object categories across studies (Joseph, 2001
; Kanwisher et al., 1997
). Faces represent the extreme end of a structural similarity continuum in that they share the same overall structure of two eyes, two ears, a nose, and a mouth (Arguin, Bub, & Dudek, 1996
; Bruce & Humphreys, 1994
; Damasio, Damasio, & Van Hoesen, 1982
). Mid-fusiform activation is not reserved only for the class of faces (Rogers et al., 2005
; Joseph & Gathers, 2002
; Gauthier et al., 1999
), thus it is important to explore a more basic principle, such as fine differentiation of structural descriptions, which may drive activation in the fusiform gyrus.
Whereas some studies have implicated the mid-fusiform gyrus in processing of shape descriptions and other studies have implicated the mid-fusiform in the process of fine differentiation of object descriptions, no studies have integrated such findings into a unified processing account. The novel contribution of the present study is the integration of findings that the mid-fusiform gyrus not only processes abstract shape representations but that these pre-semantic representations are important for making fine differentiations among visually similar objects. We presently define the “mid-fusiform” gyrus based on Joseph’s (2001)
review of category-specific brain activations in which the mid-fusiform gyrus was defined by a y
Talairach coordinate (Talairach & Tournoux, 1988
) ranging from −41 to −70. Fusiform regions outside of this range will be referred to as “anterior” or “posterior” fusiform regions.
Three major questions guided the present research. First, does the mid-fusiform gyrus process structural or perceptual descriptions of objects? Second, is the mid-fusiform gyrus involved in fine differentiation of objects at the structural or perceptual level? Third, is activation in the mid-fusiform gyrus driven by specific stimulus properties or the process of differentiating objects at the level of structural descriptions? Object recognition was measured by performance on a matching task that required deciding whether two stimuli were the same or different. Line drawings of nameable objects and 3-D shapes () were presumed to tap into processing of structural descriptions, whereas line configurations and the color information in line drawings were presumed to tap into perceptual but not structural processing. Matching of objects may also involve semantic processing, but it is not required for the matching task (in , semantic processing is parenthesized). The degree of structural and perceptual similarity between nonmatching stimuli was parametrically varied as in Joseph and Farley (2004)
and Joseph and Gathers (2003)
to tap into the process of fine differentiation. Higher levels of similarity were expected to induce higher functional magnetic resonance imaging (fMRI) signal in brain regions involved in fine differentiation.
Figure 1 Sample stimuli used in all three experiments. In Experiments 1 and 2, P stimuli tapped into perceptual processing and PS and PSS stimuli tapped into structural processing. Within each processing type, three similarity levels were manipulated (S1–S3). (more ...)
The first question is whether the process of differentiation in the mid-fusiform gyrus occurs at the level of perceptual or structural object descriptions. According to some theories of object recognition, structural descriptions specify the 3-D volumetric configuration of individual parts of an object (Biederman, 1987
; Marr & Nishihara, 1978
). The arrangement and relative sizes of the primitive components define the structure of an object. A structural description is an abstract representation that mediates between perceptual and semantic processing. It allows the visual system to map different images or exemplars of an object onto the same percept, which is critical for accessing the relatively more stable and unchanging semantic representation of an object. Perceptual descriptions, in contrast, specify the edges in an image as well as the layout of surfaces (e.g., primal and 2 1/2-D sketches; Marr, 1982
), but they do not specify the 3-D volumetric configuration of an object as structural descriptions do. Starrfelt and Gerlach (2007)
, Gerlach, Law, and Paulson (2006)
, and Gerlach et al. (2002)
have suggested that mid-fusiform regions are involved in the process of shape configuration, defined as the integration of visual elements into whole objects. Mid-fusiform regions may also process 3-D structure that is not necessarily associated with meaningful objects (Op de Beeck, Beatse, Wagemans, Sunaert, & Van Hecke, 2000
; Schacter et al., 1995
). In addition, Hayworth and Biederman (2006)
recently showed that anterior aspects of the lateral occipital complex (Malach et al., 1995
) do not respond to local image features, but instead, this region responds to the component parts of an object, which is a critical aspect of a structural description. Therefore, mid-fusiform regions may be engaged by stimuli or tasks that involve processing the structural, rather than perceptual, descriptions of objects. The first hypothesis of the present study was that objects, 3-D shapes, and processing of shape information in colored drawings were expected to induce more mid-fusiform activation than processing of line configurations or color information.
The second question is whether making fine distinctions among visually similar objects is specifically associated with mid-fusiform activation (Rogers et al., 2005
; Gerlach, Law, & Paulson, 2004
; Joseph & Farley, 2004
; Joseph & Gathers, 2003
; Price, Noppeney, Phillips, & Devlin, 2003
; Gauthier et al., 1999
; Gerlach, Law, Gade, & Paulson, 1999
; Damasio, Grabowski, Tranel, Hichwa, & Damasio, 1996
). Objects within the same category tend to overlap at the level of structural descriptions; consequently, the process of fine differentiation of objects (e.g., distinguishing different breeds of dogs) will require making fine distinctions among structural descriptions. Differentiating objects at a more basic or intermediate level may proceed from perceptual information such as the presence of straight or curved edges which may support, for example, the differentiation of natural versus manufactured objects. The present study explored this possibility further by parametrically varying the degree of similarity among objects at both the structural and perceptual levels. Two previous studies (Joseph & Farley, 2004
; Joseph & Gathers, 2003
) showed that fMRI signal in the mid-fusiform gyrus is parametrically modulated by degree of structural similarity between objects. Specifically, fMRI signal increased as the degree of structural similarity between two objects increased. This indicates that the mid-fusiform gyrus is engaged when making fine distinctions among similar objects. The finding by Rogers et al. (2005)
that the mid-fusiform gyrus is engaged when classifying objects at a more specific level is also in line with this idea. However, previous studies have not determined whether making fine distinctions among object representations occurs at the perceptual or structural level. The second hypothesis of the present study was that the brain regions that are implicated in structural processing will also show greater modulation by structural similarity than by perceptual similarity. Specifically, greater degrees of structural similarity (Similarity level 3; ) are expected to induce higher levels of activation in the mid-fusiform gyrus, whereas greater degrees of perceptual similarity are not.
The third question is whether mid-fusiform activation during fine discrimination of objects is process- or stimulus-driven. Rogers et al. (2005)
showed that the very same vehicle stimuli that engaged the mid-fusiform gyrus during specific categorization (e.g., distinguishing BMW from Morris) did not engage the mid-fusiform during intermediate categorization (e.g., distinguishing cars from dogs). Consequently, mid-fusiform activation during object processing is not driven by a specific configuration of visual features. Experiment 3 used colored line drawings and required matching based on the shape or color information as a way to control perceptual input while varying demands on structural (shape-matching) or perceptual (color-matching) processing. The third hypothesis of the present study was that shape matching will engage the mid-fusiform gyrus more strongly than will color matching.