A common neural substrate for language production and verbal working memory

Abstract

Verbal working memory (VWM), the ability to maintain and manipulate representations of speech sounds over short periods, is held by some influential models to be independent from the systems responsible for language production and comprehension [e.g., Baddeley, A. D. Working memory, thought, and action. New York, NY: Oxford University Press, 2007]. We explore the alternative hypothesis that maintenance in VWM is subserved by temporary activation of the language production system [Acheson, D. J., & MacDonald, M. C. Verbal working memory and language production: Common approaches to the serial ordering of verbal information. Psychological Bulletin, 135, 50-68, 2009b]. Specifically, we hypothesized that for stimuli lacking a semantic representation (e.g., nonwords such as mun), maintenance in VWM can be achieved by cycling information back and forth between the stages of phonological encoding and articulatory planning. First, fMRI was used to identify regions associated with two different stages of language production planning: the posterior superior temporal gyrus (pSTG) for phonological encoding (critical for VWM of nonwords) and the middle temporal gyrus (MTG) for lexical-semantic retrieval (not critical for VWM of nonwords). Next, in the same subjects, these regions were targeted with repetitive transcranial magnetic stimulation (rTMS) during language production and VWM task performance. Results showed that rTMS to the pSTG, but not the MTG, increased error rates on paced reading (a language production task) and on delayed serial recall of nonwords (a test of VWM). Performance on a lexical-semantic retrieval task (picture naming), in contrast, was significantly sensitive to rTMS of the MTG. Because rTMS was guided by language production-related activity, these results provide the first causal evidence that maintenance in VWM directly depends on the long-term representations and processes used in speech production.

Figure 1

Stimulation locations for each subject in this study, transformed to a common atlas space (ICBM 452) for display purposes. Average MNI coordinates for the pSTG stimulation were −64, −38, −13, and for the MTG, −69, −39, −2.

Figure 2

Pictorial depiction of the picture naming, paced reading, and delayed serial recall tasks used in concert with rTMS. Each figure contains the timeline over which the stimuli and rTMS pulses were delivered for each task.

Figure 3

Mean error proportions (95% CI) for paced reading as a function of region and rTMS condition. rTMS of the pSTG, but not the MTG, increased item ordering errors; no effect was observed for item omissions.

Figure 4

Mean error proportions (95% CI) for delayed serial recall as a function of region and rTMS condition. rTMS of the pSTG, but not the MTG, led to an increase in item omission errors; no effect was observed for item ordering errors.

Figure 5

Mean picture naming latency and speaking duration (95% CI) as a function of region and rTMS condition. rTMS speeded both measures, and the magnitude of this effect was numerically larger for MTG than the pSTG.