Anterior Temporal Cortex and Semantic Memory: Reconciling Findings from Neuropsychology and Functional Imaging
Rogers, Timothy T., Hocking, Julia, Noppeney, Uta, Mechelli, Andrea, et al., Cognitive, Affective and Behavioral Neuroscience
Studies of semantic impairment arising from brain disease suggest that the anterior temporal lobes are critical for semantic abilities in humans; yet activation of these regions is rarely reported in functional imaging studies of healthy controls performing semantic tasks. Here, we combined neuropsychological and PET functional imaging data to show that when healthy subjects identify concepts at a specific level, the regions activated correspond to the site of maximal atrophy in patients with relatively pure semantic impairment. The stimuli were color photographs of common animals or vehicles, and the task was category verification at specific (e.g., robin), intermediate (e.g., bird), or general (e.g., animal) levels. Specific, relative to general, categorization activated the antero-lateral temporal cortices bilaterally, despite matching of these experimental conditions for difficulty. Critically, in patients with atrophy in precisely these areas, the most pronounced deficit was in the retrieval of specific semantic information.
Studies of patients with semantic impairment suggest that the most anterior portions of the temporal cortices critically support human conceptual knowledge. The purest documented semantic syndrome, semantic dementia (SD; Hodges, Patterson, Oxbury, & Funnell, 1992; Snowden, Goulding, & Neary, 1989), arises from progressive deterioration of the anterior temporal cortex, frequently more pronounced in the left hemisphere, but always involving both (Davies, Graham, Xuereb, Williams, & Hodges, 2004; Mummery et al., 2000). Patients with SD are impaired on any task requiring knowledge about the meanings of words and objects, including picture naming, word-picture matching, category and property verification (Rogers et al., 2004; Rogers, Watling, Hodges, & Patterson, 2005; Snowden et al., 1989;Warrington, 1975), matching pictures or words on the basis of thematic associations (Hodges, Graham, & Patterson, 1995), sorting words or pictures (Hodges et al., 1992; Rogers etal., 2004), drawing-to-name and delayed copying of drawings of familiar objects (Bozeat et al., 2003; Rogers et al., 2004), sound-picture matching (Bozeat, Lambon Ralph, Patterson, Garrard, & Hodges, 2000), demonstrating the correct use of objects (Hodges, Bozeat, Lambon Ralph, Patterson, & Spatt, 2000), object reality decision (Rogers, Lambon Ralph, Hodges, & Patterson, 2003), and so on (see Patterson & Hodges, 2000). These deficits are typically observed for all semantic categories (Garrard, Lambon Ralph, & Hodges, 2002) and are apparent in all modalities of testing but are specific to semantic knowledge; other cognitive faculties are reasonably well preserved in the disorder (Hodges, Garrard, & Patterson, 1998). The striking consistency of both the cognitive and the neural abnormalities in SD strongly suggests that the bilateral anterior temporal cortices are critical for amodal and domain-general aspects of semantic processing (Rogers et al., 2004); that is, they contribute to semantic processing for all kinds of concepts and for all modalities of reception and expression. In line with this view, other brain diseases that can affect the anterior temporal lobes (ATLs), such as Alzheimer's disease and herpes simplex viral encephalitis, also often disrupt semantic memory, although never as selectively as in SD (Hodges & Patterson, 1995).
Functional neuroimaging has offered a rather startlingly different picture of the neural representation of semantic knowledge, in three respects. First, the majority of research has yielded left-sided, rather than bilateral, cortical activations for semantic tasks (Devlin et al., 2002; Joseph, 2001; Martin & Chao, 2001; Thompson-Schill, 2003). second, functional imaging results have indicated that semantic knowledge is encoded in a widely distributed cortical network, with different regions specialized to represent particular kinds of information (Martin & Chao, 2001; Tranel, Damasio, & Damasio, 1997), particular categories of object (Caramazza & Mahon, 2003; Perani et al. …