Verb generation in patients with focal frontal lesions: A neuropsychological test of neuroimaging findings

Abstract

What are the neural bases of semantic memory? Traditional beliefs that the temporal lobes subserve the retrieval of semantic knowledge, arising from lesion studies, have been recently called into question by functional neuroimaging studies finding correlations between semantic retrieval and activity in left prefrontal cortex. Has neuroimaging taught us something new about the neural bases of cognition that older methods could not reveal or has it merely identified brain activity that is correlated with but not causally related to the process of semantic retrieval? We examined the ability of patients with focal frontal lesions to perform a task commonly used in neuroimaging experiments, the generation of semantically appropriate action words for concrete nouns, and found evidence of the necessity of the left inferior frontal gyrus for certain components of the verb generation task. Notably, these components did not include semantic retrieval per se.One of the earliest findings in cognitive neuroimaging was that the left inferior frontal gyrus (IFG) is activated when subjects are shown a concrete noun and must generate a semantically appropriate verb (1-5). This finding, which now has been replicated many times, has been interpreted as evidence that the left IFG plays a role in the retrieval of semantic knowledge. This interpretation is supported by other neuroimaging studies finding left IFG activation during different tasks requiring semantic retrieval, such as living͞nonliving classification (6-8). In contrast, the literature on cognitive impairments after focal brain lesions reveals no particular association between semantic retrieval and left prefrontal cortex (9). Patients with prefrontal lesions have normal language comprehension; although lesions to either left or right prefrontal cortex do impair the ability to generate semantically related words on a category fluency task, they also impair performance in nonsemantic fluency tasks (10), consistent with an underlying impairment that is not semantic per se (11). Impairments of semantic knowledge are most associated with temporal lobe, not frontal lobe, pathology (12)(13)(14).In this paper, we consider two possible explanations for the discrepancy between the findings from neuroimaging and neuropsychological studies of the role of prefrontal cortex in semantic retrieval. First, differences in the outcomes from these two types of studies may reflect simply the different types of inferences to which neuroimaging studies and lesion studies lend themselves. Neuroimaging studies are limited to inferences about brain regions that are engaged by a cognitive process as revealed by correlated changes in activity related to processing demands. In contrast, a neuropsychological approach allows one to make inferences about brain regions that are necessary for a cognitive process, when that process can be shown to depend on the integrity of a given brain region (15). Thus, one interpretation of the neuroimaging findings that can be tested in patients with frontal...

Meta‐analyses of object naming: Effect of baseline

“…Specifically, Lambon Ralph et al [2001] have proposed that object-naming difficulties after anterior temporal lobe damage (including temporal poles, anterior fusiform, and parahippocampal cortices) can be explained solely in terms of a semantic impairment, and De Renzi et al [1987] have proposed that object-naming difficulties after left posterior inferior temporal damage can be explained in terms of deficits transmitting visual information to the speech areas. Thompson-Schill et al [1998] have proposed that the left posterior inferior frontal cortex is necessary for a nonsemantic selection process that is engaged when there are many sources of competing information [see Kan and Thompson-Schill, 2004]. In addition, right cerebellar metabolism [Feeney and Baron, 1986] and structure [Price et al, 1999] are known to be intricately connected to that in the left inferior frontal cortex and therefore may also play a role in response selection.…”

The human brain representation of odor identification

“…Indeed, the fusiform and inferior temporal gyri are under top-down control of the inferior frontal gyrus, which was also more active during OI. The inferior frontal gyrus actively guides retrieval and selection of the correct representation (Badre et al 2005;Gough et al 2005;Thompson-Schill et al 1998;Wig et al 2005). Activity in the left inferior temporal gyrus (Kareken et al 2003) and inferior frontal gyrus has been reported previously in OI and odor name-ability studies (Suzuki et al 2001;Zelano et al 2009).…”

“…OI also engaged secondary olfactory regions such as the orbitofrontal cortex. Brain areas connected to representation, retrieval, and selection of semantic representations, such as the posterior temporal lobe and inferior frontal gyrus (Badre et al 2005;Binder et al 2009;Bookheimer 2002;Gough et al 2005;Thompson-Schill et al 1998;Wig et al 2005), were also particularly engaged by OI. The OI and PS results support the idea that neuronal correlates of odor processing are task dependent, involving both olfactory core regions and a distributed network of structures outside of this determined by the Fig.…”

“…However, piriform and orbitofrontal cortices may also play a role, since they are involved in odor categorization and higher-order odor associative activity (Anderson et al 2003;Cerf-Ducastel and Murphy 2003;Li et al 2010;Schoenbaum and Eichenbaum 1995). In addition, the network supporting semantic processing in the posterior temporal lobe and ventrolateral prefrontal cortex (Badre et al 2005;Binder et al 2009;Bookheimer 2002;Gough et al 2005;Thompson-Schill et al 1998;Wig et al 2005) is expected to participate in OI. To test this prediction, we performed an uncued odor functional magnetic resonance imaging (fMRI) study of brain activity in response to spontaneously identified vs. nonidentified odors as determined postscanning.…”

Sources of individual differences in the speed of naming objects and actions: The contribution of executive control

“…The deficits include working memory capacity and inhibiting ability. Moreover, evidence suggests that brain-damaged patients with deficient inhibiting abilities have difficulty producing words under conditions of high lexical competition in a word generation task (e.g., Badre, Poldrack, Paré-Blagoev, Insler, & Wagner, 2005;Thompson-Schill et al, 1998). Studies of ADHD have indicated that deficient inhibiting abilities caused disfluencies during sentence production (e.g., Engelhardt, Corley, Nigg, & Ferreira, 2010).…”