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Research Articles, Behavioral/Cognitive

Spatially-specific working memory activity in the human superior colliculus

Masih Rahmati, Kevin DeSimone, Clayton E. Curtis and Kartik K. Sreenivasan
Journal of Neuroscience 28 October 2020, JN-RM-2016-20; https://doi.org/10.1523/JNEUROSCI.2016-20.2020
Masih Rahmati
1Department of Psychology, New York University, New York, NY 10003, USA
2Division of Science and Mathematics, New York University Abu Dhabi, Abu Dhabi, UAE
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Kevin DeSimone
1Department of Psychology, New York University, New York, NY 10003, USA
2Division of Science and Mathematics, New York University Abu Dhabi, Abu Dhabi, UAE
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Clayton E. Curtis
1Department of Psychology, New York University, New York, NY 10003, USA
3Center for Neural Science, New York University, New York, NY 10003, USA
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Kartik K. Sreenivasan
2Division of Science and Mathematics, New York University Abu Dhabi, Abu Dhabi, UAE
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Abstract

Theoretically, working memory (WM) representations are encoded by population activity of neurons with distributed tuning across the stored feature. Here, we leverage computational neuroimaging approaches to map the topographic organization of human superior colliculus (SC) and model how population activity in SC encodes WM representations. We first modeled receptive field properties of voxels in SC, deriving a detailed topographic organization resembling that of the primate SC. Neural activity within human (5 male and 1 female) SC persisted throughout a retention interval of several types of modified memory-guided saccade tasks. Assuming an underlying neural architecture of the SC based on its retinotopic organization, we used an encoding model to show that the pattern of activity in human SC represents locations stored in WM. Our tasks and models allowed us to dissociate the locations of visual targets and the motor metrics of memory-guided saccades from the spatial locations stored in WM, thus confirming that human SC represents true WM information. These data have several important implications. They add the SC to a growing number of cortical and subcortical brain areas that form distributed networks supporting WM functions. Moreover, they specify a clear neural mechanism by which topographically organized SC encodes WM representations.

SIGNIFICANCE STATEMENT

Using computational neuroimaging approaches, we mapped the topographic organization of human superior colliculus (SC) and modeled how population activity in SC encodes working memory (WM) representations, rather than simpler visual or motor properties that have been traditionally associated with the laminar maps in the primate SC. Together, these data both position the human SC into a distributed network of brain areas supporting WM and elucidate the neural mechanisms by which the SC supports WM.

Footnotes

  • The authors declare no competing financial interests.

  • We thank Jeffrey Kravitz for processing and analyzing the eye tracking data. We thank New York University’s Center for Brain Imaging for technical support. We thank Martin Paré for helpful discussions about the research study. This research was supported by the National Eye Institute (R01 EY-016407 and R01 EY-027925 to C.E. Curtis) and by an NYU Global Seed Grants for Collaborative Research (K.K. Sreenivasan and C.E. Curtis).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

SfN exclusive license.

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Spatially-specific working memory activity in the human superior colliculus
Masih Rahmati, Kevin DeSimone, Clayton E. Curtis, Kartik K. Sreenivasan
Journal of Neuroscience 28 October 2020, JN-RM-2016-20; DOI: 10.1523/JNEUROSCI.2016-20.2020

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Spatially-specific working memory activity in the human superior colliculus
Masih Rahmati, Kevin DeSimone, Clayton E. Curtis, Kartik K. Sreenivasan
Journal of Neuroscience 28 October 2020, JN-RM-2016-20; DOI: 10.1523/JNEUROSCI.2016-20.2020
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