Role of the left inferior frontal gyrus in covert word retrieval: Neural correlates of switching during verbal fluency

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Abstract

Word retrieval ability is commonly assessed with a semantic verbal fluency task, in which subjects must produce a list of exemplars of a category (e.g., animals). The order in which exemplars are produced is not random; rather, subjects tend to produce “clusters” of semantically related items (e.g., cow, pig, sheep) and occasionally “switch” to other clusters (e.g., lion, tiger, bear). Patients with frontal lobe pathology (associated with focal lesions or Parkinson's disease) exhibit reduced output on semantic fluency tasks that has been characterized as a reduction in switching, in contrast to other impaired patient groups who produce normal switches but smaller clusters (e.g., [Troyer, A. K., Moscovitch, M., Winocur, G., Leach, L., & Freedman, M. (1998). Clustering and switching on verbal fluency tests in Alzheimer's and Parkinson's disease. Journal of the International Neuropsychological Society, 4(2), 137–143]). The ability to initiate a switch between two semantic categories may require the selection of weakly activated representations over active (but already reported) representations. Previous studies have shown that increased demands on selection among competing representations are associated with activity in the left inferior frontal gyrus (LIFG) and with deficits in patients with lesions including LIFG [Thompson-Schill, S. L., Jonides, J., Marshuetz, C., Smith, E. E., D’Esposito, M., Kan, I. P., et al. (2002). Effects of frontal lobe damage on interference effects in working memory. Cognitive Affective & Behavioral Neuroscience, 2(2), 109–120; Thompson-Schill, S. L., Swick, D., Farah, M. J., D’Esposito, M., Kan, I. P., & Knight, R. T. (1998). Verb generation in patients with focal frontal lesions: A neuropsychological test of neuroimaging findings. Proceedings of the National Academy of Sciences of the United States of America, 26, 14792–14797]. In the present study, we investigated the neural correlates of switching in the verbal fluency task, and in particular, the role of the LIFG in switching between semantic sub-categories. We observed greater activation in the LIFG during switching compared to free generation (Experiment 1) and self-reported clustering (Experiment 2), which is consistent with the hypothesis that the switching mechanism is subserved by the LIFG due to high semantic selection demands.

Section snippets

Participants

Ten paid subjects participated (three males and seven females), mean age 22.8 years. All participants were right-handed, native English speakers (i.e., did not learn another language before age 6 years). Participants were also screened for neurological and neuropsychological illnesses, use of psychoactive medications and learning differences (e.g., dyslexia). Participation consisted of a 1 h session. Participants gave informed consent and were compensated with US$ 20.

Materials

A total of 40 category names

Participants

Nine paid subjects participated (four males and five females), mean age 23.1 years; none of these subjects were in Experiment 1. All participants were right-handed, native English speakers (did not learn another language before age 6 years). Participants were also screened for neurological and neuropsychological illnesses, use of psychoactive medications and learning differences (e.g., dyslexia). Participation consisted of a 1 h session. Participants gave informed consent and were compensated

General discussion

The present findings from Experiments 1 and 2 are consistent with the hypothesis that the LIFG subserves processes that support switching between sub-categories during semantic verbal fluency. Notably, in the group random effects analysis, pars triangularis (BA 45) was more highly activated during switching tasks than free generation (Experiment 1) and self-reported clustering (Experiment 2). Activation in BA 45 has been implicated in tasks where verbal responses to stimuli activate many

Summary

Numerous studies have shown ventrolateral PFC involvement during a variety of verbal (Jonides et al., 1998, Kan et al., 2005; Thompson-Schill et al., 2002, Thompson-Schill et al., 1998) and non-verbal tasks (Brandon, Hirshorn, Jha, Fabian, & Thompson-Schill, 2004) where performance requires overriding a highly activated representation or selecting among weakly activated, incompatible representations. We propose that switching during verbal fluency is another instance of a response that depends

Acknowledgements

This research was supported by NIH RO167008 and the Searle Scholars Program. A preliminary version of this study was reported at the annual Human Brain Mapping meeting in 2004. We would like to thank Geoffrey K. Aguirre, Julia C. Lemos and J. Stephen Higgins for their help in the design and analysis of this study. Correspondence regarding this manuscript should be addressed to Sharon L. Thompson-Schill, Department of Psychology, University of Pennsylvania, 3720 Walnut Street B-51, 19104.

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