The two fMRI experiments reported in this chapter presented evidence for a „new‟ category- selective region responsive to vision of hands in human extrastriate visual cortex. Hand-selective responses were strongest in the anterior portion of the left lateral occipital sulcus. Two experiments demonstrated the functional preference of this region to hands relative to various control conditions, including feet and fingers that share several features with hands (fingers are part of the hand and feet have five toes). The hand response was localised anterior and closely adjacent to non-hand body responses. Interestingly, contrary to EBA, the hand response in the LOS was strongly left lateralised. Indeed, all 14 participants showed a hand response in the left hemisphere whereas only 6 participants also showed a similar activation in the right hemisphere. These findings are in line with previous evidence reporting the existence of (1) hand-selective cells in monkey IT (Desimone, et al., 1984; Gross, et al., 1969), (2) a larger number of hand-responsive ERP sites in the human left temporal lobe (McCarthy, et al., 1999) and (3) hand vs. torso specificity in the human visual cortex using fMRI (Op de Beeck, et al., 2010). Finally, the present data provide the first evidence for a double dissociation in the lateral occipitotemporal cortex between the representations of a specific body part such as hands in the left LOS (where activation for hands was higher than both whole-bodies and body-parts) and bodies in general in the nearby left EBA (where activation for both whole-body and body-parts were higher than hands). Indeed, while previous work (Op de Beeck, et al., 2010) showed higher activation for hands as compared to torsos and faces in the lateral occipitotemporal cortex, it did not find significantly greater responses to torsos than hands - a preferred response to torsos as compared to hands was reported only in the right fusiform gyrus. The selective response to hands but not torsos is in agreement with our findings, and suggests that hands more than other body parts are selectively represented in the lateral occipitotemporal cortex.
What do our results suggest about the organisation of body part representations in the human lateral occipitotemporal cortex? One possibility is that selective representations exist for some, or perhaps all, individual body parts, with the EBA being the collection of these separate representations (Orlov, et al., 2010). Alternatively, the hand, similar to the face, could be a
“special” body part and distinctive among other body parts in eliciting selective responses in the
human high-order visual cortex. Indeed, the way we interact with co-specifics and with the external world is continuously mediated by our hands, starting with learning how to intake food, following by pointing at objects to name them, continuing with learning how to count and write, and then
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developing into more complex abilities such as gesture communication and tool-use execution/understanding. In light of the special role played by hands in our daily experience it is therefore not surprising that hands, like faces, are selectively represented in visual cortex relative to other body parts. However, it should be pointed out that, despite the absence of a selective response to feet and fingers in the current study, we cannot rule out that a less conservative contrast (for instance feet versus chairs and fingers versus chairs) would uncover such responses. Finally, future experiments using high-resolution fMRI (Schwarzlose, Baker, & Kanwisher, 2005) and fMRI adaptation will be useful to test for the existence of separate body part representations within EBA and the extrastriate visual cortex more generally (as initially reported in Orlov, et al., 2010).
Regardless of whether the hand response in left LOS is a unique functional region or should instead be considered a sub-region of EBA, it clearly shows a distinct functional specialisation in the present studies. The left LOS, but not EBA, responded to non-human robotic hands and partially to non-biological stimuli such as tools, but not to other objects such as chairs. This response profile may relate to recent findings suggesting a broader modulation of neural activity in visual areas from other modalities, such as semantics (Mahon, et al., 2009), tactile information (Amedi, et al., 2001; Burton, Snyder, Diamond, & Raichle, 2002) and motor action (Astafiev, Stanley, Shulman, & Corbetta, 2004). In this respect, the human‟s unique manual abilities to manipulate external objects and tools might influence the information encoded within left LOS. The relevance of occipitotemporal regions in storing not only visual object information, but also motion and associated action knowledge with it, gained support in a series of experiments by Beauchamp and colleagues (Beauchamp, et al., 2002, 2003). These reports showed that while an area in the posterior part of the superior temporal lobe (STS) anterior and superior to the motion area MT (Grossman, et al., 2000; Grossman & Blake, 2002) responds to body-related form and motion, a region within the posterior middle temporal gyrus (MTG) anterior and inferior to MT responds to tool-associated form and motion (Beauchamp, et al., 2002, 2003). Interestingly, anterior to left LOS in the left MTG a selective response to tools has been widely reported (Chao, et al., 1999; Valyear, et al., 2007; Valyear & Culham, 2009), but see also Downing and co-workers (Downing, et al., 2006). A number of imaging studies support the role of left MTG in coding not only the visual form of tool but also conceptual knowledge and tool-associated actions (Binder, Desai, Graves, & Conant, 2009; Devlin, et al., 2002; Martin, Haxby, Lalonde, Wiggs, & Ungerleider, 1995; Martin, et al., 1996). In support of these findings, clinical studies (Tranel, et al., 1997; Tranel, Kemmerer, Adolphs, Damasio, & Damasio, 2003) showed that lesions involving left
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MTG cause impairments in action knowledge associated with objects. In this respect, the observation that left LOS, but not EBA, responds to tools may reflect a coding of motion information of hand actions associated with tool use.
Interestingly, in contrast to the predominantly right hemispheric lateralisation of other visual body and face selective regions, such as FBA (Peelen & Downing, 2005), FFA (Kanwisher, et al., 1997), OFA (Puce, et al., 1996) , and EBA itself (Downing, et al., 2001), the hand response in LOS showed a strong left hemispheric lateralisation. Neural mechanisms encoding hands being primarily lateralised in the hemisphere dominant for human praxis suggests an advantageous structural organisation that allows fast inter-hemispheric connections between brain regions in left occipitotemporal cortex representing hand visual form, hand motion, and tool-actions, and left frontoparietal regions subserving planning and guidance of hand actions (Goodale & Milner, 1992; Rizzolatti, Luppino, & Matelli, 1998). In line with this, clinical studies report that while left frontoparietal and parietal lesions frequently induce postural and spatial temporal errors in gesture imitation and object usage (Buxbaum & Saffran, 2002; Haaland, Harrington, & Knight, 2000), lesions within the left temporo-parietal junction compromise the conceptual knowledge of the correct hand movements associated with a specific object (De Renzi & Lucchelli, 1988). An interesting avenue for future research is to test the role of left LOS in the observation and execution of object-directed hand actions, and to investigate functional connectivity between the hand- selective region and other regions implicated in these processes (e.g., left lateralised frontoparietal action network). Indeed, the body is not a passive entity but mediates our interaction with the external world. This bidirectional interactive experience is likely to be critical in modulating and shaping functional brain organisation.
In conclusion, the experiments reported in this chapter provide evidence for neural representation of the human hand in the left occipitotemporal cortex. EBA has generally been regarded as a uniform neural substrate dedicated to visual body processing. These results indicate that segregated body-part representations may exist within the lateral occipitotemporal cortex, with the hand being selectively represented relative to other body parts. Interestingly, the left LOS hand- selective region (unlike the nearby body-selective region) showed stronger activation to inanimate tools relative to the other inanimate object category (chairs). Although hands and tools differ in many respects such as visual appearance (e.g., shape, colour and texture) and object domain (i.e. animate vs. inanimate), nevertheless they are functionally linked with each other via common involvement in action-related processing (i.e. object interaction and object manipulation).
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Therefore, (1) the necessity to send visual information about hands and tools to the left lateralized praxic system to subserve action-related processing together with (2) functional connectivity constraints that exist between the praxic system and the visual cortex might force visual processing of hands and tools within corresponding anatomical locations in high order visual cortex. In support of this hypothesis, evidence for left lateralised representation for both hands (Bracci, et al., 2010) and tools (previously reported in Chao, et al., 1999), suggest a possible role of the left lateralised praxis system in driving this hemispheric specialisation. In other words, functional connectivity between the visual system and the functionally specialised frontoparietal action- related network may constrain localisation of hand-selective and tool-selective representations in the left LOTC. Both the issue of possible overlap between selective activation for hands and tools and the issue of possible modulation by the action system need further exploration.
The relevance of these issues is as follows. If previously reported activation for visual depictions of tools overlaps with visual depictions of hands, then this would question the nature of such activation. Visual activation for tools (as well as bodies, faces etc.) is generally thought to reflect visual recognition and identification. Overlapping selectivity for both tools and hands would suggest instead relevance to praxis rather than visual recognition. Such functional organisation of high-order cortex to reflect non-visual object dimensions would provide novel insight into the organisation of the visual cortex with potential far reaching implication for our understanding of the visual system. Although we found a suggestion of overlap between activation for hands and tools in the findings reported in this chapter, such overlap needs to be assessed in much more detail in order to provide firm evidence. Furthermore, rather than demonstrating mere overlap and speculating about how this may reflect non-visual object dimensions in the visual system, it is desirable to find evidence for a more direct link to praxis, such as modulation of the visual system by downstream action systems. These two aims form the basis of the rationale for Study 2 reported in this thesis. In the next experimental chapter I will report investigation on (1) functional and anatomical association between hand-selective responses found within left LOS and the nearby tool-selective area (left MTG-TA, as reported by Chao et al. 1999); (2) the role of functional connectivity between the visual system and areas part of the action-related network in driving functional specialisation of hand-selective and tool-selective areas in the left occipitotemporal cortex.
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