Paradoxical response reversal of top-down modulation in cortical circuits with three interneuron types
Abstract
Pyramidal cells and interneurons expressing parvalbumin (PV), somatostatin (SST), and vasoactive intestinal peptide (VIP) show cell type-specific connectivity patterns leading to a canonical microcircuit across cortex. Experiments recording from this circuit often report counterintuitive and seemingly contradictory findings. For example, the response of SST cells in mouse V1 to top-down behavioral modulation can change its sign when the visual input changes, a phenomenon that we call response reversal. We developed a theoretical framework to explain these seemingly contradictory effects as emerging phenomena in circuits with two key features: interactions between multiple neural populations and a nonlinear neuronal input-output relationship. Furthermore, we built a cortical circuit model which reproduces counterintuitive dynamics observed in mouse V1. Our analytical calculations pinpoint connection properties critical to response reversal, and predict additional novel types of complex dynamics that could be tested in future experiments.
Article and author information
Author details
Funding
Office of Naval Research (N00014-17-1-2041)
- Xiao-Jing Wang
Science and Technology Commission of Shanghai Municipality (14JC1404900)
- Xiao-Jing Wang
NIH Blueprint for Neuroscience Research (R01MH062349)
- Xiao-Jing Wang
Science and Technology Commission of Shanghai Municipality (15JC1400104)
- Xiao-Jing Wang
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2017, Garcia del Molino et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,087
- views
-
- 573
- downloads
-
- 62
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.