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Articles, Systems/Circuits

A Brain System for Auditory Working Memory

Sukhbinder Kumar, Sabine Joseph, Phillip E. Gander, Nicolas Barascud, Andrea R. Halpern and Timothy D. Griffiths
Journal of Neuroscience 20 April 2016, 36 (16) 4492-4505; DOI: https://doi.org/10.1523/JNEUROSCI.4341-14.2016
Sukhbinder Kumar
1Auditory Group, Institute of Neuroscience, Medical School, Newcastle University, Newcastle upon Tyne NE2 4HH, United Kingdom,
2Wellcome Trust Centre for Neuroimaging, London WC1N 3BG, United Kingdom,
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Sabine Joseph
3Institute of Cognitive Neuroscience, London, United Kingdom,
4Institute of Neurology, UCL Neuroscience, London WC1N 3AR, United Kingdom,
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Phillip E. Gander
5Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa 52242,
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Nicolas Barascud
6UCL Ear Institute, London WC1X 8EE, United Kingdom, and
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Andrea R. Halpern
7Department of Psychology, Bucknell University, Lewisburg, Pennsylvania 17837
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Timothy D. Griffiths
1Auditory Group, Institute of Neuroscience, Medical School, Newcastle University, Newcastle upon Tyne NE2 4HH, United Kingdom,
2Wellcome Trust Centre for Neuroimaging, London WC1N 3BG, United Kingdom,
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  • Figure 1.
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    Figure 1.

    Working memory paradigm. After a pair of tones was presented, subjects were cued to maintain one of the two tones in working memory for 16 s. A decision period followed in which subjects compared a probe tone with the tone in working memory.

  • Figure 2.
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    Figure 2.

    Activity in the auditory cortex during encoding, maintenance, and retrieval phases of the working memory task. A, Results of univariate analyses at the individual voxel level for encoding (top), maintenance (middle), and retrieval (bottom) phases. Activity is thresholded at p = 0.05, corrected for multiple comparisons for the volume of auditory cortex. B, Comparison of activity in different ROIs of the auditory cortex for encoding (top), maintenance (middle), and retrieval (bottom) phases. C, Time series from different ROIs of auditory cortex. Med, Medial; Mid, middle; Lat, lateral.

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    Figure 3.

    Activity in hippocampus during encoding, maintenance, and retrieval phases of the working memory task. A, Results of univariate analysis at the individual voxel level for encoding (top), maintenance (middle), and retrieval (bottom) phases. Activity is thresholded at p = 0.05 corrected for multiple comparisons for the volume of hippocampus. B, Activity for the three phases of the working memory task along the anterior–posterior axis of left hippocampus (top) and right hippocampus (bottom). This is done by calculating the average activity of all voxels within hippocampus at a given value of y-coordinate. The y-coordinate is changed from anterior to posterior (y = −8 to −38) at 2 mm resolution. C, Time series plot of activity in the anterior and posterior hippocampus in left hemisphere (i) and right hemisphere (ii).

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    Figure 4.

    Activity in the left and right IFG for the encoding, maintenance, and retrieval phases of the working memory task. Ai, Results of univariate analysis at the individual voxel level overlayed on the structural scan. Peaks of activity in the left and right IFG are marked with white circles. Activity is thresholded at p = 0.05 corrected for multiple comparisons for the whole brain. Aii, Plots of β values at the peak voxels in left and right IFG during the encoding, maintenance, and retrieval phases. Aiii, Time series plots at the peak voxels of left and right IFG. Bi, A more dorsal–anterior (than shown in Ai) location in the right IFG that only responds during the retrieval phase. Plots of β values (Bii) and time series (Biii) at that locus are shown.

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    Figure 5.

    A–C, Correlation of BOLD activity with behavioral performance accuracy during the encoding (A), maintenance (B), and retrieval (C) phases. Voxels with significant correlation with behavioral performance were identified using p = 0.001 (uncorrected). Ai, Aii, Positive correlation during encoding is observed in rTPJ (Ai) and STG/STS (Aii). Bi–Biv, Positive correlation during maintenance in parietal cortex (Bi); negative correlation during maintenance in DMN (Bii), hippocampus (Biii), and IFJ (Biv). Ci, Negative correlation during retrieval in retrosplenial cortex. For display purposes, β values overlaid in the MRI structural scan during encoding, maintenance and retrieval are thresholded at p = 0.01 (uncorrected), p = 0.001 (uncorrected) and p = 0.001 (uncorrected) respectively.

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    Figure 6.

    Percentage accuracy of pattern classification (low vs high tone) during the maintenance period using MVPA. The mean (±SEM across subjects) classifier performance is shown. Chance performance is 50% (marked horizontal line). Accuracy is above chance level in the HG (p = 0.001) and left IFG (p = 0.016).

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    Figure 7.

    Analysis of connectivity among auditory cortex, IFG, and hippocampus. Connectivity is compared during the three phases of the working memory task. i, Encoding vs maintenance, p = 0.05 (corrected). ii, Retrieval > encoding (p = 0.05 (corrected). No connection was significant for encoding > retrieval. There was no significant difference (in either direction) for retrieval vs maintenance contrast.

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    Table 1.

    List of brain areas that are activated during the maintenance period

    Name of regionBrodmann area numberMNI coordinates of the peak/subpeakst Value of the peak/subpeaksNumber of voxels in the cluster
    Right supplementary motor areaBA64, 16, 4615.22622
    −2, 2, 6012.29
    14, 18, 4412.13
    Left inferior frontal gyrusBA44−50, 6, 015.11201
    −58, 6, 1610.11
    Right anterior cingulateBA3210, 26, 3214.8535
    Left superior parietalBA40−48, −28, 4814.611114
    −48, −20, 5212.29
    −48, −50, 5011.97
    Right insula/inferior frontal gyrusBA1330, 24, 212.66281
    60, −14, 412.07
    52, 8, 010.16
    Left PT/STG−58, −46, 1612.6642
    Left pons−2, −24, −4011.4967
    Left anterior insulaBA13−32, 16, 810.66296
    −30, 24, 410.42
    −36, 16, 010.29
    Left inferior parietalBA7−24, −66, 4610.0477
    Left premotorBA6−30, −4, 629.7520
    Left cerebellum−36, −56, −509.4624
    Left frontal poleBA11−24, 44, −149.3215
    Left medulla−4, −38, −489.235
    Left frontalBA9−54, 8, 309.1128
    Left posterior temporal lobe−34, −56, 129.116
    Right cerebellum28, −54, −368.9012
    Right posterior STGBA4146, −36, 168.7912
    Right posterior temporal lobe38, −60, 28.795
    Left superior frontal−24, 4, 668.778
    Right somatosensory/motor areaBA1, BA2, BA354, −24, 528.4918
    Thalamus−10, −16, 08.356
    Left frontalBA9−50, 4, 408.335
    Right superior parietalBA4040, −46, 448.297
    • The activations (with respect to silent period as baseline) are thresholded at p = 0.05 (corrected for multiple comparisons for the whole brain volume). Only clusters with a size ≥5 voxels are listed. Any subpeaks present in the cluster are also mentioned (peaks are shown in bold letters and subpeaks in nonbold letters).

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The Journal of Neuroscience: 36 (16)
Journal of Neuroscience
Vol. 36, Issue 16
20 Apr 2016
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A Brain System for Auditory Working Memory
Sukhbinder Kumar, Sabine Joseph, Phillip E. Gander, Nicolas Barascud, Andrea R. Halpern, Timothy D. Griffiths
Journal of Neuroscience 20 April 2016, 36 (16) 4492-4505; DOI: 10.1523/JNEUROSCI.4341-14.2016

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A Brain System for Auditory Working Memory
Sukhbinder Kumar, Sabine Joseph, Phillip E. Gander, Nicolas Barascud, Andrea R. Halpern, Timothy D. Griffiths
Journal of Neuroscience 20 April 2016, 36 (16) 4492-4505; DOI: 10.1523/JNEUROSCI.4341-14.2016
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Keywords

  • auditory cortex
  • fMRI
  • hippocampus
  • MVPA
  • working memory

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