Premorbid expertise produces category-specific impairment in a domain-general semantic disorder

Abstract

For decades, category-specific semantic impairment – i.e., better comprehension of items from one semantic category than another – has been the driving force behind many claims about the organisation of conceptual knowledge in the brain. Double dissociations between patients with category-specific disorders are widely interpreted as showing that different conceptual domains are necessarily supported by functionally independent systems. We show that, to the contrary, even strong or classical dissociations can also arise from individual differences in premorbid expertise. We examined two patients with global and progressive semantic degradation who, unusually, had known areas of premorbid expertise. Patient 1, a former automotive worker, showed selective preservation of car knowledge, whereas Patient 2, a former botanist, showed selective preservation of information about plants. In non-expert domains, these patients showed the typical pattern: i.e., an inability to differentiate between highly similar concepts (e.g., rose and daisy), but retention of broader distinctions (e.g., between rose and cat). Parallel distributed processing (PDP) models of semantic cognition show that expertise in a particular domain increases the differentiation of specific-level concepts, such that the semantic distance between these items resembles non-expert basic-level distinctions. We propose that these structural changes interact with global semantic degradation, particularly when expert knowledge is acquired early and when exposure to expert concepts continues during disease progression. Therefore, category-specific semantic impairment can arise from at least two distinct mechanisms: damage to representations that are critical for a particular category (e.g., knowledge of hand shape and action for the category ‘tools’) and differences in premorbid experience.