Searching for the elusive neural substrates of body part terms: A neuropsychological study

Abstract

Previous neuropsychological studies suggest that, compared to other categories of concrete entities, lexical and conceptual aspects of body part knowledge are frequently spared in brain-damaged patients. To further investigate this issue, we administered a battery of 12 tests assessing lexical and conceptual aspects of body part knowledge to 104 brain-damaged patients with lesions distributed throughout the telencephalon. There were two main outcomes. First, impaired oral naming of body parts, attributable to a disturbance of the mapping between lexical-semantic and lexical-phonological structures, was most reliably and specifically associated with lesions in the left frontal opercular and anterior/inferior parietal opercular cortices and in the white matter underlying these regions (8 patients). Also, 1 patient with body part anomia had a left occipital lesion that included the “extrastriate body area” (EBA). Second, knowledge of the meanings of body part terms was remarkably resistant to impairment, regardless of lesion site; in fact, we did not uncover a single patient who exhibited significantly impaired understanding of the meanings of these terms. In the 9 patients with body part anomia, oral naming of concrete entities was evaluated, and this revealed that 4 patients had disproportionately worse naming of body parts relative to other types of concrete entities. Taken together, these findings extend previous neuropsychological and functional neuroimaging studies of body part knowledge and add to our growing understanding of the nuances of how different linguistic and conceptual categories are operated by left frontal and parietal structures.

Keywords:

• Body parts
• Embodied cognition
• Broca's area
• Inferior parietal lobule
• Extrastriate body area

We thank Ken Manzel for assistance with data collection, Kathy Jones and Ruth Henson for help with scheduling the participants, Joel Bruss from Thomas Grabowski's Computational Neuroimaging Laboratory for help with Figure 3, and Asifa Majid for many fruitful discussions about the linguistic encoding of body parts. This work was supported in part by Program Project Grant, National Institute of Neurological Disorders and Stroke, NINDS P01 NS19632.

Notes

¹ Another region with body-specific response properties was recently found in the posterior fusiform gyrus, partially overlapping the “fusiform face area” (Peelen & Downing, 2005a; Peelen et al., 2006; Schwartzlose, Baker, & Kanwisher, 2005). This region, called the “fusiform body area” (FBA), is biased toward the perception of complete body images, whereas the EBA is biased toward the perception of body parts (Taylor, Wiggett, & Downing, 2007).

² The meanings of body part terms may also include various kinds of “encyclopaedic” information, but we do not address such knowledge in this study.

³ Kosslyn (2006, p. 1521) expresses this point as follows, alluding to neuroanatomical hypotheses that we delineate more fully in the section “Hypotheses”: “Consider the spatial relation between the forearm and upper arm when a person assumes different postures. If that relation is described as ‘connected by a hinge,’ the same spatial relation applies when the arm is bent a little bit, straight, or bent more than 90º—or when it is at any other angle. Thus, if the forearm and upper arm are described as ‘connected by a hinge’ (with the parts being recognized in the ventral system and the spatial relation produced in the dorsal system), outputs from the ventral and dorsal systems can produce the same descriptions for different contortions of the form….”

⁴ The numbers “3” and “1” indicate lexical tones.

⁵ BA stands for Brodmann area, and we use the conventional numbering system.

⁶ We do not address written word production in this study.

⁷ See also Kiani, Esteky, Mirpour, and Tanaka (2007), who recorded the responses of a large number (>600) of neurons in monkey ventral temporal cortex to a large number (>1,000) of natural and artificial object images. The investigators found that the cells have complex activation patterns, or population codes, that capture the hierarchical organization of object forms, with an overarching division between animate and inanimate objects and multiple nested subdivisions within the global category of animate objects, including faces—further split into primate and nonprimate faces—and bodies—further split into human bodies, four-limb animal bodies, other animal bodies (insects, fish, reptiles), and hands.

⁸ It is noteworthy, however, that pure heterotopagnosia—a very rare disorder—is more subtle than this. For instance, when heterotopagnosic participants fail to point to the named body parts of other people, their errors usually involve self-referencing—that is, pointing to the corresponding body parts on themselves, while simultaneously making odd statements like “Your mouth … is my mouth”, which suggest a disturbance of self–other differentiation (Degos, Bachoud-Levi, Ergis, Petrissans, & Cesaro, 1997). Moreover, they can accurately point to the named body parts of inanimate human images, such as dolls, and they can also accurately reach out and grasp the named body parts of other people, suggesting that they are only impaired when the task involves pointing to the named body parts of an animate, conscious person who has his/her own visuospatial perspective on the participant's gestural behaviour (Degos et al., 1997; Felician et al., 2003).

⁹ This test was motivated in part by the fact that in some languages body part terms are used much more frequently and productively than in English to designate the parts of inanimate objects, and the choice of terms is determined in a rule-governed fashion by visuospatial analyses of axial and contour features. Perhaps the best-studied language of this type is Tzeltal, in which even an object as seemingly nondescript as a stone may be assigned a “face”, a “nose”, an “ear”, a “back”, a “belly”, or any of about 15 other quasi-metaphorical body parts—for example, an s-jol “head” is a protrusion that is located at one end of the major axis of an object and that has a gently curved, circular outline with only minor concavities on either side (Brown, 2006; Levinson, 1994; see also Heine, 1997).

¹⁰ The stimuli and target words used in this follow-up study were not matched with those used in the body part naming study according to nuisance variables like object familiarity, object complexity, word frequency, and age of word acquisition. In general, though, our normal comparison data indicate that the overall difficulty of the two sets of stimuli (body parts, other concrete entities) is very similar, with normal performances falling in the mid-90s percentage correct. Thus, a direct comparison is valid.