Role of left inferior prefrontal cortex in retrieval of semantic knowledge: A reevaluation

Abstract

A number of neuroimaging findings have been interpreted as evidence that the left inferior frontal gyrus (IFG) subserves retrieval of semantic knowledge. We provide a fundamentally different interpretation, that it is not retrieval of semantic knowledge per se that is associated with left IFG activity but rather selection of information among competing alternatives from semantic memory. Selection demands were varied across three semantic tasks in a single group of subjects. Functional magnetic resonance imaging signal in overlapping regions of left IFG was dependent on selection demands in all three tasks. In addition, the degree of semantic processing was varied independently of selection demands in one of the tasks. The absence of left IFG activity for this comparison counters the argument that the effects of selection can be attributed solely to variations in degree of semantic retrieval. Our findings suggest that it is selection, not retrieval, of semantic knowledge that drives activity in the left IFG.What parts of the brain subserve the retrieval of semantic knowledge? A number of recent neuroimaging studies, using a range of different tasks, implicate the left inferior frontal gyrus (IFG) (1-8). Despite the impressive convergence of localizations across tasks as disparate as verb generation, stem completion, and abstract͞concrete judgments, the conclusion that semantic retrieval critically involves left IFG remains uncertain for two reasons. First, a smaller but still significant number of neuroimaging studies have failed to find left IFG activation during semantic retrieval tasks. For example, neither naming pictures nor verifying word associations consistently leads to left IFG activation, despite the prima facie involvement of semantic knowledge in both tasks (9, 10). Additionally, practice of a semantic retrieval task, even after just a single repetition, causes a marked decrease in left IFG activation (2,8). Second, neuropsychological studies of patient populations have so far failed to demonstrate the necessity of left IFG for semantic retrieval. Instead, impairments of semantic knowledge are most associated with temporal lobe pathology (11-13).The goal of this article is to propose and test an alternative interpretation of the activation of left IFG during semantic retrieval tasks, based on recent theorizing about the role of prefrontal cortex in nonsemantic domains. Cohen and ServanSchreiber (14) argued that prefrontal cortex enables flexible and context-sensitive responses, particularly in tasks where a response other than the prepotent one must be selected. Kimberg and Farah (15) characterized the role of prefrontal cortex in cognition as mediating the selection of action by the weighting of information active in working memory. When the contents of working memory are not critical for action selection, because the action is prepotent, or when the contents of working memory overwhelming support one action, then demands on prefrontal cortex are low. Their model implies that demands on pre...

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“…This explanation is consistent with the finding that the retrieval and selection of semantic features has been associated with left inferior prefrontal activity in hemodynamic (e.g. [66]) as well as ERP [48] investigations. Whereas individuals differ in the types of strategies they will spontaneously use when faced with challenging tasks, it is currently unclear whether the group differences we observed could have been reduced by providing instructions as to how to encode the items, for example, by using a deep, semantic encoding task (see e.g.…”

“…Consistent with the role of the left PFC for semantic retrieval processes [66,48], during source memory retrieval this region has been implicated in two important control operations. The first is the specification of relevant semantic retrieval cues based on the features of the potential sources (i.e.…”

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“…However, these dissociations are somewhat complicated by the fact that certain brain structures underlying the procedural system also play specific roles related to declarative memory. Ventro-lateral pre-frontal cortex, which corresponds to the inferior frontal gyrus and BA 44, 45 and 47 (Damasio, 1995), underlies the encoding of new declarative memories and the selection or retrieval of declarative knowledge (Buckner, 2000;Buckner and Wheeler, 2001;Thompson-Schill et al, 1997;Wagner et al, 1998).…”

“…However, these dissociations are somewhat complicated by the fact that certain brain structures underlying the procedural system also play specific roles related to declarative memory. Ventro-lateral pre-frontal cortex, which corresponds to the inferior frontal gyrus and BA 44, 45 and 47 (Damasio, 1995), underlies the encoding of new declarative memories and the selection or retrieval of declarative knowledge (Buckner, 2000;Buckner and Wheeler, 2001;Thompson-Schill et al, 1997;Wagner et al, 1998).Moreover, evidence suggests that portions of the basal ganglia and the cerebellum are also involved in 12 selecting, retrieving or searching for declarative memories (Desmond and Fiez, 1998;Ivry and Fiez, 2000; Ullman, in press-a;Wise et al, 1996). Thus the DP model predicts that these structures should play analogous functional roles for lexical memory -namely, in the selection, retrieval or search for lexical knowledge (Ullman, in press-a).…”