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Articles, Behavioral/Cognitive

Frontal–Medial Temporal Interactions Mediate Transitions among Representational States in Short-Term Memory

Derek Evan Nee and John Jonides
Journal of Neuroscience 4 June 2014, 34 (23) 7964-7975; DOI: https://doi.org/10.1523/JNEUROSCI.0130-14.2014
Derek Evan Nee
1Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720, and
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John Jonides
2Department of Psychology, University of Michigan, Ann Arbor, Michigan 48109
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  • Figure 1.
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    Figure 1.

    Task and hypothesized states. A, Depiction of the task. The task required participants to hold several digits in STM and perform simple arithmetic. During encoding, digits were presented within colored frames. The frames served as contexts for the items. After a retention interval, colored frames indicated that digits that had appeared in those frames would be candidates for operation. For each operation, participants applied the operation to the digit associated with the frame, responded with the solution via a key press, and updated STM with the result. When the second operation of a pair indicated a different item than the first, the focus of attention in STM had to be switched (focus switch). By contrast, when the same item was operated upon twice in a row, the focus remained fixed (focus repeat). After a pair of operations, participants could be cued to either the same set (active repeat; not depicted) or different set (active switch; depicted). This was followed by another pair of operations. Finally, participants recalled all of the digits. B, Hypothesized states of STM at the time in between the second pair of operations. All digits reflect the updated contents of STM after operations have been applied. Having just applied “+3” to the digit “6” associated with the lower left frame, the frame-digit (“9”) pair are expected to be the focus of attention (green). All digits that are candidates for operation (red circles) are hypothesized to be held in an active state in which digits are bound to their contexts (red dashed links). By contrast, items that are not candidates for operation are held in an unbound, passive state (blue circles).

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    Figure 2.

    Behavioral results. A, Greater reaction times (RT) were associated with larger active set sizes. However, no difference was observed between passive set size 2 (Pasv2) and 3 (Pasv3). These data indicate a representational state distinction between the active and passive sets. B, Greater RTs were associated with switching the focus of attention relative to when the focus of attention was repeated on the same item confirming a cost in switching the focus of attention. C, Switching the active set incurred a cost relative to repeating the active set on the first operation following a switch (Op2.1), but not the second (Op2.2). These data indicate a transient cost of switching the active set. D, The focus switch cost (Foc Sw Cost) increased as a function of the active set size, but not the passive set size. These data indicate that switches of the focus are affected by competition within the active set confirming that the focus acts within the active, but not passive, state. †p < 0.05 (one-tailed). *p < 0.05. **p < 0.005. ***p < 0.0005.

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    Figure 3.

    Univariate results. A, Areas showing greater activation for the focus switch > focus repeat contrast. These areas included the cSFS in the vicinity of the frontal eye fields, an area involved in top-down attention. B, Areas showing greater activation for the active switch > active repeat contrast. These areas included the PMv, a region involved in articulatory rehearsal. C, Direct comparisons of focus switch (focus switch − focus repeat) and active switch (active switch − active repeat) contrasts within ROIs. ROIs were created using a leave-1-subject-out procedure and thus provided an unbiased estimate of effect size. Both the right and left cSFS showed significant focus switch, but not active switch effects. The left and right PMv showed a significant active switch, but not focus switch effect. For full statistics and interaction tests, see Univariate fMRI results. *p < 0.05. **p < 0.005. ***p < 0.0005.

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    Figure 4.

    Functional connectivity interactions. A, Functional connectivity interactions with the right cSFS. Only interactions with the right MTL survived family-wise error correction for this contrast. Correlation data are plotted within an ROI based upon previous literature, thereby providing an unbiased estimate of effect sizes. Interactions between the right cSFS and anterior hippocampus (ant hipp) were driven both by greater cSFS-ant hipp connectivity during focus switches relative to focus repeats and a trend toward reduced cSFS-ant hipp connectivity during active switches relative to active repeats. B, Functional connectivity interactions with the left PMv. Correlation data are plotted within an ROI based upon previous literature, thereby providing an unbiased estimate of effect sizes. Interactions between the left PMv and posterior hippocampus (pos hipp) were driven mainly by significantly greater PMv-pos hipp connectivity during active switches relative to active repeats. †p < 0.05 (one-tailed). *p < 0.05.

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    Figure 5.

    Connectivity gateways. A, Functional connectivity interactions for the contrast of (focus switch − focus repeat) − (active switch − active repeat) with the cSFS (green) and ant hipp (red). A conjunction was observed in the right posterior parietal cortex, indicating that this area may be a gateway between the cSFS and ant hipp. B, Functional connectivity interactions for the contrast of active switch − active repeat with the PMv (blue) and pos hipp (red). Conjunctions were observed in the PFC, indicating that these areas may be gateways between the PMv and pos hipp.

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    Figure 6.

    Model of frontal–medial temporal interactions. Three representational states of STM are hypothesized to be the focus (green), active state (red), and passive state (blue). A, The focus is mediated by the cSFS serving as attention to an item-context pair. The active state consists of item-context bindings that are mediated by the MTL. Passive items are not bound to their context. B, An operation to be performed on a different digit than the last serves as a cue to switch the focus. The cue is contextual, so the focus is first switched to the corresponding context. C, Focus on a context can activate a corresponding item through bindings mediated by the MTL. In this way, the cSFS and MTL work in concert to focus a new item-context pair. D, A cue to switch the active state results in the rehearsal of previously passive items through the action of the PMv. As a consequence, the focus is disrupted because the item-context pair to which it was attending is no longer active. E, Rehearsal of items triggers links to the MTL, which are in turn propagated to contexts enabling retrieval of item-context bindings. Thus, the PMv and MTL work in concert to change the active state.

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    Table 1.

    Univariate resultsa

    ContrastXYZNo. of voxelsTBARegion
    Focus switch > focus repeat66507736.326Right preSMA
    02585.066PreSMA
    −610484.7632Left ACC
    30−6481355.086Right cSFS
    44−8541074.916Right PMd
    −42226834.7544Left IFJ
    −4420161734.7245Left IFG-tria
    −4610124.5444Left IFG-oper
    −342283.8213Left ant insula
    −36−8541814.476Left PMd
    −38−16424.244Left preCG
    −42−4503.746Left PMd
    8−74−41054.4418Left lingual gyrus
    −6−80−123.9317Right lingual gyrus
    Focus repeat > focus switch56−28−67265.5521Right MTG
    52−50105.4221Right MTG
    56−4044.222Right STG
    60−52302335.3740Right SMG, AG
    −52−6830834.1639Left AG
    −40−70323.9819Left MOG
    Active switch > active repeat−604302415.666Left PMv
    −56−10444.094Left preCG
    −52−8363.884Left preCG
    −6−70222185.4218Left calcarine
    −6−72−43.9518Left lingual gyrus
    −14−60123.5317Left calcarine
    • ↵aResults from unvariate contrasts. All coordinates reported in MNI space. ACC, Anterior cingulate cortex; AG, angular gyrus; ant, anterior; BA, Brodmann's area; IFG-oper, inferior frontal gyrus, pars opercularis; IFG-tria, inferior frontal gyrus, pars triangularis; IFJ, inferior frontal junction; MTG, middle temporal gyrus; MOG, middle occipital gyrus; PMd, dorsal premotor cortex; PMv, ventral premotor cortex; preCG, precentral gyrus; preSMA, presupplemental motor area; SMG, supramarginal gyrus; STG, superior temporal gyrus.

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    Table 2.

    Functional connectivity interactionsa

    Seed/contrastXYZNo. of voxelsTBARegion
    cSFS seed (focus switch − focus repeat) − (active switch − active repeat)22−8−242333.6236Right PHG
    20−10−163.19Right ant hipp
    PMv seed (active switch − active repeat) − (focus switch − focus repeat)−22−28−183513.1830Left PHG
    −26−26−82.82Left pos hipp
    −28−22−222.6930Left PHG
    • ↵aResults from functional connectivity interactions. All coordinates reported in MNI space. ant, Anterior; BA, Brodmann's area; hipp, hippocampus; PHG, parahippocampal gyrus; PMv, ventral premotor cortex; pos, posterior.

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The Journal of Neuroscience: 34 (23)
Journal of Neuroscience
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4 Jun 2014
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Frontal–Medial Temporal Interactions Mediate Transitions among Representational States in Short-Term Memory
Derek Evan Nee, John Jonides
Journal of Neuroscience 4 June 2014, 34 (23) 7964-7975; DOI: 10.1523/JNEUROSCI.0130-14.2014

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Frontal–Medial Temporal Interactions Mediate Transitions among Representational States in Short-Term Memory
Derek Evan Nee, John Jonides
Journal of Neuroscience 4 June 2014, 34 (23) 7964-7975; DOI: 10.1523/JNEUROSCI.0130-14.2014
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Keywords

  • fMRI
  • focus of attention
  • frontal cortex
  • hippocampus
  • medial temporal lobe
  • working memory

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