Generalization of learned responses in the mormyrid electrosensory lobe
- Columbia University, United States
Abstract
Appropriate generalization of learned responses to new situations is vital for adaptive behavior. We provide a circuit-level account of generalization in the electrosensory lobe (ELL) of weakly electric mormyrid fish. Much is already known in this system about a form of learning in which motor corollary discharge signals cancel responses to the uninformative input evoked by the fish's own electric pulses. However, for this cancellation to be useful under natural circumstances, it must generalize accurately across behavioral regimes, specifically different electric pulse rates. We show that such generalization indeed occurs in ELL neurons, and develop a circuit-level model explaining how this may be achieved. The mechanism involves regularized synaptic plasticity and an approximate matching of the temporal dynamics of motor corollary discharge and electrosensory inputs. Recordings of motor corollary discharge signals in mossy fibers and granule cells provide direct evidence for such matching.
Data availability
Data and model code are available via Zenodo (doi: 10.5281/zenodo.2590782).
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Data and model associated withZenodo, doi:10.5281/zenodo.2590782.
Article and author information
Author details
Funding
National Science Foundation (1025849)
- Larry F Abbott
- Nathaniel Sawtell
National Institute of Neurological Disorders and Stroke (NS075023)
- Nathaniel Sawtell
Irma T. Hirschl Trust
- Nathaniel Sawtell
Simons Foundation
- Larry F Abbott
Gatsby Charitable Foundation
- Larry F Abbott
National Science Foundation (1707398)
- Larry F Abbott
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All experiments performed in this study adhere to the American Physiological Society's Guiding Principles in the Care and Use of Animals and were approved by the Columbia University Institutional Animal Care and Use Committee, protocol AAAW4462.
Copyright
© 2019, Dempsey 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.
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Generalization of learned responses in the mormyrid electrosensory lobe
eLife 8:e44032.
https://doi.org/10.7554/eLife.44032
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- 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.
