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Manipulating stored phonological input during verbal working memory


Verbal working memory (vWM) involves storing and manipulating information in phonological sensory input. An influential theory of vWM proposes that manipulation is carried out by a central executive while storage is performed by two interacting systems: a phonological input buffer that captures sound-based information and an articulatory rehearsal system that controls speech motor output. Whether, when and how neural activity in the brain encodes these components remains unknown. Here we read out the contents of vWM from neural activity in human subjects as they manipulated stored speech sounds. As predicted, we identified storage systems that contained both phonological sensory and articulatory motor representations. Unexpectedly, however, we found that manipulation did not involve a single central executive but rather involved two systems with distinct contributions to successful manipulation. We propose, therefore, that multiple subsystems comprise the central executive needed to manipulate stored phonological input for articulatory motor output in vWM.

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Figure 1: Match–mismatch task.
Figure 2: Example responses.
Figure 3: Subdivisions of delay activity.
Figure 4: Idealized and representative responses.
Figure 5: Representation of vWM.
Figure 6: Error analysis: during the delay epoch, all four response classes differentiated between trials with a correct utterance and trials with no utterance (chance is 0.5; dotted red lines).

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We thank A. Weiss, J. MacArthur and L. Frank for developing the data acquisition hardware and software, E. Londen, P. Purushothaman, C. Boomhaur, and P. Minhas for technical assistance, and C. Curtis for comments on the manuscript. This work was supported, in part, by R03-DC010475 from the NIDCD, an Award from the Simons Collaboration for the Global Brain (B.P.).

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Authors and Affiliations



G.B.C. designed the experiment, performed the research, analyzed the data and wrote the manuscript. A.I. performed the research and analyzed the data. L.M. performed the research and wrote the manuscript. T.T. performed the research. O.D. performed the research and wrote the manuscript. D.F. and W.D. performed the research. B.P. designed the experiment, performed the research, analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Bijan Pesaran.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Localization of responses

a. For each subject, we classified neural activity using an electrode’s response to a localizer task (see Experimental Procedures). Auditory (green), indicates an electrode responded to incoming sensory stimuli, Production (blue) indicates that an electrode responded to the motor output during the response, and Sensory-Motor (red) indicates that an electrode responded to both the incoming sensory stimuli and the motor production. Delay responses were also present in each electrode category (Delay+ - Purple outline) as well as Delay-Only Responses (Purple). b. Localization of electrodes across subjects. Color convention the same as in a.

Supplementary Figure 2 Example responses.

a. Example spectrograms of the neural responses for non-delay Electrodes. An Auditory electrode (top row) during the remembered sensory-motor dissociation task: A high gamma (70 Hz +) neural response is seen in the auditory epoch but not during the delay epoch. In an example Production electrode (second row) Significant neural activity is present in the production epoch but not during the delay period. In an example Sensory-Motor electrode (third row) significant neural activity is seen in the auditory and production epochs, but not during the delay. Note that the gray bar reflects the variable delay period (1.5 – 2 seconds post auditory onset). b. Average high gamma power traces (70 – 160 Hz) are shown for each electrode class as shown in a: Auditory, Production, and Sensory-Motor. c. Localization of each spectrogram from Fig 3a (left column) and Fig S2a (right column). Error values are SEM of power across electrodes (Auditory: N = 23 Electrodes, Production: N = 34, Sensory-Motor: N = 8).

Supplementary Figure 3 Example spectrograms for each class and subject.

We show for example spectrograms for each subject for each delay electrode type (where present).

Supplementary Figure 4 Representations of non-vWM responses.

Using the same models and procedure as illustrated in Fig 5, we demonstrate the representations of each non-delay electrode category. While the patterns are very similar to their Delay counterparts, crucially there is an absence of delay representations.

Supplementary Figure 5 A leave-one-out analysis.

We repeat our classifier/model analysis (see Fig 5) using iterations of our subject pool with a single subject removed and compare it to the entire subject pool. Removing some subjects weakened the effects, but the representation of vWM in each electrode class was qualitatively the same, indicating that our results are not due to a single subject effect. Delay+Auditory sites tended to encode in an Audtory representation. Delay+Production sites tended to encode in a Motor representation. Delay+Sensory-motor sites tended to encode in a Sensory-Motor representation. The Delay-only sites tended to encode in a Rule representation.

Supplementary information

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Supplementary Figures 1–5 and Supplementary Tables 1–3 (PDF 1247 kb)

Supplementary Methods Checklist (PDF 430 kb)

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Cogan, G., Iyer, A., Melloni, L. et al. Manipulating stored phonological input during verbal working memory. Nat Neurosci 20, 279–286 (2017).

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