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Attention selectively reshapes the geometry of distributed semantic representation

Samuel A. Nastase, Andrew C. Connolly, Nikolaas N. Oosterhof, Yaroslav O. Halchenko, J. Swaroop Guntupalli, Matteo Visconti di Oleggio Castello, Jason Gors, M. Ida Gobbini, James V. Haxby
doi: https://doi.org/10.1101/045252
Samuel A. Nastase
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
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  • For correspondence: samuel.a.nastase.gr@dartmouth.edu
Andrew C. Connolly
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
2Department of Neurology, Geisel School of Medicine at Dartmouth, Hanover, NH 03755
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Nikolaas N. Oosterhof
3Centerfor Mind/Brain Sciences, Universitá degli studi di Trento, 38068 Rovereto, Italy
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Yaroslav O. Halchenko
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
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J. Swaroop Guntupalli
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
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Matteo Visconti di Oleggio Castello
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
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Jason Gors
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
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M. Ida Gobbini
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
4Department of Medicina Specialistica, Diagnostica e Sperimentale (DIMES), Medical School, University of Bologna, 40126 Bologna, Italy
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James V. Haxby
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755
3Centerfor Mind/Brain Sciences, Universitá degli studi di Trento, 38068 Rovereto, Italy
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Abstract

Humans prioritize different semantic qualities of a complex stimulus depending on their behavioral goals. These semantic features are encoded in distributed neural populations, yet it is unclear how attention might operate across these distributed representations. To address this, we presented participants with naturalistic video clips of animals in their natural environments while they attended to either behavior or taxonomy. We used models of representational geometry to investigate how attentional allocation affects the distributed neural representation of animal behavior and taxonomy. Attending to animal behavior transiently increased the discriminability of distributed population codes for observed actions in anterior intraparietal, pericentral, and ventral temporal cortices, while collapsing task-irrelevant taxonomic information. Attending to animal taxonomy while viewing the same stimuli increased the discriminability of distributed animal category representations in ventral temporal cortex and collapsed behavioral information. For both tasks, attention selectively enhanced the categoricity of response patterns along behaviorally relevant dimensions. These findings suggest that behavioral goals alter how the brain extracts semantic features from the visual world. Attention effectively disentangles population responses for downstream read-out by sculpting representational geometry in late-stage perceptual areas.

Significance Humans can extract different kinds of high-level information from the visual world depending on their behavioral goals. Here, we use naturalistic stimuli and simple models of neural representation to investigate whether attention affects how the brain encodes semantic information. When paying attention to the behavior of an animal in its natural environment, for example, the neural representation of the observed action becomes more distinct, while irrelevant information about taxonomy is collapsed. Attending to taxonomy, on the other hand, has the inverse effect. These attentional effects occur primarily in late-stage sensorimotor areas ratherthan in early sensory areas. Overall, our behavioral goals dynamically alter how the brain processes the semantic qualities of a stimulus to better encode important information.

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Posted March 23, 2016.
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Attention selectively reshapes the geometry of distributed semantic representation
Samuel A. Nastase, Andrew C. Connolly, Nikolaas N. Oosterhof, Yaroslav O. Halchenko, J. Swaroop Guntupalli, Matteo Visconti di Oleggio Castello, Jason Gors, M. Ida Gobbini, James V. Haxby
bioRxiv 045252; doi: https://doi.org/10.1101/045252
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Attention selectively reshapes the geometry of distributed semantic representation
Samuel A. Nastase, Andrew C. Connolly, Nikolaas N. Oosterhof, Yaroslav O. Halchenko, J. Swaroop Guntupalli, Matteo Visconti di Oleggio Castello, Jason Gors, M. Ida Gobbini, James V. Haxby
bioRxiv 045252; doi: https://doi.org/10.1101/045252

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