Award Abstract # 1615737
Robust spatiotemporal dynamics in multi-layer neuronal networks

NSF Org: DMS
Division Of Mathematical Sciences
Recipient: THE REGENTS OF THE UNIVERSITY OF COLORADO
Initial Amendment Date: August 19, 2016
Latest Amendment Date: August 19, 2016
Award Number: 1615737
Award Instrument: Standard Grant
Program Manager: Junping Wang
jwang@nsf.gov
 (703)292-4488
DMS
 Division Of Mathematical Sciences
MPS
 Directorate for Mathematical and Physical Sciences
Start Date: September 1, 2016
End Date: August 31, 2019 (Estimated)
Total Intended Award Amount: $234,000.00
Total Awarded Amount to Date: $234,000.00
Funds Obligated to Date: FY 2016 = $234,000.00
History of Investigator:
  • Zachary Kilpatrick (Principal Investigator)
    zpkilpat@colorado.edu
Recipient Sponsored Research Office: University of Colorado at Boulder
3100 MARINE ST
Boulder
CO  US  80309-0001
(303)492-6221
Sponsor Congressional District: 02
Primary Place of Performance: University of Colorado at Boulder
CO  US  80309-0526
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): SPVKK1RC2MZ3
Parent UEI:
NSF Program(s): MATHEMATICAL BIOLOGY
Primary Program Source: 01001617DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 8091
Program Element Code(s): 733400
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.049

ABSTRACT

To navigate in a constantly changing world, humans and other animals continually make decisions and store memories. Since the world is noisy and brain activity is highly variable, it is remarkable that organisms can perform cognitive tasks as accurately as they do. One feature of the human brain that may account for its exceptional computational ability is its modular structure. The entire network of the brain is organized into a collection of densely connected subnetworks, helping to localize certain neural computations. Studying the effects of this underlying structure could ultimately help in the analysis of increasingly large data sets collected by experimental neuroscientists. This project will consider the impact of modular structures in the brain, focusing on networks known to perform specific cognitive tasks like categorization, short-term memory, and spatial navigation. These computations are performed by networks that can represent spatial position, and the associated mathematical models often describe variables that change in space and time. This project will facilitate the development of new methods for studying how noise impacts the dynamics of neuronal networks with multiple temporal and spatial scales, specifically in networks with a multi-layered structure. This project will contribute to the national BRAIN initiative by identifying new computational tools for understanding the role of the brain's network architecture in cognition. Furthermore, trainees supported by this award will learn cutting-edge methods in statistics, nonlinear dynamics, and stochastic processes. These methods are broadly applicable to many fields in science that utilize large-scale data such as genetics, social science, and climatology.

This research project addresses the problem of understanding how the multi-layered structure of many areas of the brain shape neural computation. This problem will be addressed in three main ways: (i) building multi-layer network models of observed brain circuits that process spatial information; (ii) developing mathematical tools for studying these equations to extract information about their dynamics; and (iii) corroborating this work with experimental collaborators that record and image propagating activity in brain tissue. The cognitive tasks of spatial navigation, spatial working memory, and visual input categorization will be studied. Spatial navigation requires the integration of both angular and linear self-motion cues, and models developed in the project will explore different ways multi-layered network architecture can dampen variability in position codes. The investigation of how multi-layered architectures with different scales of spatial heterogeneity can robustly represent spatial position will improve our insights into the function of spatial working memory. Experimental recordings from visual brain areas have found that interfaces between network layers modify the propagation of stimulus-related activity. The impact of this phenomenon on stimulus processing will be explored in detail using mathematical models of sensory brain activity. All these projects require the development of new tools for determining how noise influences multi-scale systems, metastability, and spatiotemporal patterns, of broad applicability to other scientific fields including epidemiology, systems biology, and ecology.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 12)
AE Radillo, A Veliz-Cuba, K Josic*, and ZP Kilpatrick* "Evidence accumulation and change rate inference in dynamic environments" Neural Comput. , v.29 , 2017 , p.1561 doi:10.1162/NECO_a_00957
AE Radillo, A Veliz-Cuba, K Josi, and ZP Kilpatrick "Performance of normative and approximate evidence accumulation on the dynamic clicks task" Neurons, Behavior, Data analysis, and Theory , 2019 , p.10226 https://arxiv.org/abs/1902.01535
A Jacot-Guillarmod, Y Wang, C Pedroza, H Ogmen, ZP Kilpatrick*, and K Josic* "Extending Levelt?s Propositions to perceptual multistability involving interocular grouping" Vision Res. , v.133 , 2017 , p.37 http://dx.doi.org/10.1016/j.visres.2016.12.017
DB Poll and ZP Kilpatrick "Velocity integration in a multilayer neural field model of spatial working memory" SIAM J Appl. Dyn. Syst. , v.16 , 2017 , p.1197 https://doi.org/10.1137/16M1102471
Gregory Faye and Zachary P Kilpatrick "Threshold of front propagation in neural fields: An interface dynamics approach" SIAM J Appl. Math. , v.78 , 2018 , p.2575 https://doi.org/10.1137/18M1165797
Khanh P Nguyen, Kresimir Josic, and Zachary P Kilpatrick "Optimizing sequential decisions in the drift-diffusion model" J Math Psychol , v.88 , 2019 , p.32 https://doi.org/10.1016/j.jmp.2018.11.001
Nikhil Krishnan and Zachary P Kilpatrick "Optimizing a jump-diffusion model of a starving forager" Physical Review E , v.98 , 2018 , p.052406 10.1103/PhysRevE.98.052406
Nikhil Krishnan, Daniel B. Poll, and Zachary P. Kilpatrick "Synaptic efficacy shapes resource limitations in working memory" Journal of Computational Neuroscience , v.44 , 2018 , p.273 https://doi.org/10.1007/s10827-018-0679-7
ZP Kilpatrick "Synaptic mechanisms of interference in working memory" Scientific Reports , v.8 , 2018 , p.7879 https://doi.org/10.1038/s41598-018-25958-9
ZP Kilpatrick and DB Poll "Neural field model of memory-guided search" Phys. Rev. E , v.96 , 2017 , p.062411 https://doi.org/10.1103/PhysRevE.96.062411
ZP Kilpatrick, J Gjorgjieva, and R Rosenbaum "Editorial: Special Issue from the 2017 International Conference on Mathematical Neuroscience" J Math. Neurosci. , v.9 , 2019 , p.1 https://doi.org/10.1186/s13408-018-0069-5
(Showing: 1 - 10 of 12)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Cognitive computations are accomplished by a wide variety of complex activity dynamics in the networks of the brain. We focused specifically on the neural dynamics responsible for working memory and decision making. Working memory is the process by which pieces of information are stored for a short period of time and used to perform some calculation or computation. Decision making requires the accumulation of evidence to determine the best choice between multiple alternatives. We studied these phenomena by building neuronal network models which generated spatiotemporal activity to encode these cognitive processes.

Intellectual Merit: First, we showed how the multilayered structure of cortex is important for making these computations robust. One common working memory task developed for test animals is that of a spatial navigation task in which the subject must remember their location along a linear track. We showed that encoding position with a neural activity bump that spans multiple layers of a network can reduce encoding error that might arise due to internal noise or network variability. Moreover, we showed that such position encoding networks can be utilized to store information about previously visited locations, not just an animal's current location, when neural activity propagates as a moving front. This work also prompted further study for conditions of wave propagation in neural activity models, providing a fundamental mathematical framework for understanding propagation thresholds in nonlocal models. The idea of modeling memory for previously visited locations also springboarded additional work studying optimal strategies for animals foraging in an environment that they slowly deplete. This study pushed forward new theory on the statistics of first passage times in discrete models.

A second aim of the project was to understand how the dynamics of the synaptic connections of neural networks may shapes information storage. A key study focusing on this aim explored how short term facilitation, the process by which synapses of frequently active neurons are strengthened on the timescale of seconds, may contribute to the interaction of multiple items stored in memory over time. Interference is a commonly observed phenomenon in working memory experiments whereby previously remembered items can bias one's memory for currently stored items. We found that short term facilitation can account for this in a neuronal network model, as the facilitated synapses from previously remembered items can attract the neural activity representing the currently remembered item. Our model made a number of experimentally testable predictions concerning the behavioral responses of subjects performing back-to-back working memory trials, and potentially the neural activity recordings to be expected in non-human primates. We are currently in the process of working with experimental collaborators to test these predictions in collected behavioral data and neural recordings.

In related work, we have explored how neural activity interactions within a single trial might account for working memory item interference of simultaneously stored items. Indeed, we found that the distance between items in feature space can strongly shape the nature of item interference, in the context of a neural network model. These predictions are also being validated currently with collected behavioral data from collaborators.

We also studied how multiple layers of a network could implement adaptive decision making. A key finding was that the rate of environmental changes can be encoded by the strength of synapses between the layers which is tuned by long term plasticity. This suggests a fundamental neural mechanism for adaptive evidence integration in networks, which we are exploring currently in a subsequent funded project.

Broader impacts: These results were disseminated broadly through papers (9) in refereed applied math and neuroscience journals; conference talks and seminars; and tutorials. One tutorial was given at the International Conference on Mathematical Neuroscience in June 2019 to 60 students from all over the world, about half of whom were women. One PhD student, Daniel Poll, graduate in May 2017, and is currently a postdoc at Northwestern. Another PhD student, Kate Nguyen, will likely graduate in August 2020. Three undergraduates were funded, leading to two publications. At present, the PI is training two female students from countries underrepresented in science, a female undergraduate, and a female postdoc, so more than half of the trainees in the group are from underrepresented groups in STEM.


Last Modified: 11/12/2019
Modified by: Zachary P Kilpatrick

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