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Independent theta phase coding accounts for CA1 population sequences and enables flexible remapping.

Chadwick A, van Rossum MC, Nolan MF - Elife (2015)

Bottom Line: These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies.We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity.Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.

View Article: PubMed Central - PubMed

Affiliation: Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom.

ABSTRACT
Hippocampal place cells encode an animal's past, current, and future location through sequences of action potentials generated within each cycle of the network theta rhythm. These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies. Instead, we find through simulations and analysis of experimental data that rate and phase coding in independent neurons is sufficient to explain the organization of CA1 population activity during theta states. We show that CA1 population activity can be described as an evolving traveling wave that exhibits phase coding, rate coding, spike sequences and that generates an emergent population theta rhythm. We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity. Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.

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Remapping with coordinated assemblies.(A) Comparison of single cell phase precession generated bycoordinated assemblies (before and after remapping) and independentcoding. For this simulation, single cell phase and rate fields wereassumed to be perfectly remapped, so that any changes are purely due toassembly interactions. Note that, while assembly interactions improvephase coding in single cells in the initial environment, after remappingthese same interactions disrupt phase precession and cause a lower(circular-linear) correlation between spike phase and animal locationthan that generated by independent cells. (B) Populationfiring rate on a single trial along a linear track. While assemblyinteractions initially entrain and amplify theta oscillations in thepopulation compared to independent cells, after remapping theseinteractions disrupt theta activity and cause a lower overall activitylevel.DOI:http://dx.doi.org/10.7554/eLife.03542.019
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fig7s1: Remapping with coordinated assemblies.(A) Comparison of single cell phase precession generated bycoordinated assemblies (before and after remapping) and independentcoding. For this simulation, single cell phase and rate fields wereassumed to be perfectly remapped, so that any changes are purely due toassembly interactions. Note that, while assembly interactions improvephase coding in single cells in the initial environment, after remappingthese same interactions disrupt phase precession and cause a lower(circular-linear) correlation between spike phase and animal locationthan that generated by independent cells. (B) Populationfiring rate on a single trial along a linear track. While assemblyinteractions initially entrain and amplify theta oscillations in thepopulation compared to independent cells, after remapping theseinteractions disrupt theta activity and cause a lower overall activitylevel.DOI:http://dx.doi.org/10.7554/eLife.03542.019

Mentions: What are the advantages of independent coding compared to sequence generation throughinteractions between cell assemblies? When an animal is moved between environments,the relative locations at which place cells in CA1 fire remap independently of oneanother (e.g., O'Keefe and Conway,1978; Wilson and McNaughton,1993). This global remapping of spatial representations poses a challenge forgeneration of theta sequences through coordinated assemblies as synaptic interactionsthat promote formation of sequences in one environment would be expected to interferewith sequences in a second environment. Indeed, in the coordinated assembly model,simulations of remapping reduced single cell phase precession to below the level ofindependent cells (i.e., of an identical simulation with interactions between cellsremoved). Remapping in the coordinated coding model also substantially reduced firingrate and population oscillations (Figure7—figure supplement 1). This decrease in firing rate followingremapping contradicts experimental data showing an increase in firing rate in novelenvironments (Karlsson and Frank, 2008). Itis not immediately clear whether the independent coding model faces similarconstraints on sequence generation across different spatial representations. Wetherefore addressed the feasibility of maintaining theta sequences followingremapping given the assumptions that underpin our independent coding model.


Independent theta phase coding accounts for CA1 population sequences and enables flexible remapping.

Chadwick A, van Rossum MC, Nolan MF - Elife (2015)

Remapping with coordinated assemblies.(A) Comparison of single cell phase precession generated bycoordinated assemblies (before and after remapping) and independentcoding. For this simulation, single cell phase and rate fields wereassumed to be perfectly remapped, so that any changes are purely due toassembly interactions. Note that, while assembly interactions improvephase coding in single cells in the initial environment, after remappingthese same interactions disrupt phase precession and cause a lower(circular-linear) correlation between spike phase and animal locationthan that generated by independent cells. (B) Populationfiring rate on a single trial along a linear track. While assemblyinteractions initially entrain and amplify theta oscillations in thepopulation compared to independent cells, after remapping theseinteractions disrupt theta activity and cause a lower overall activitylevel.DOI:http://dx.doi.org/10.7554/eLife.03542.019
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4383210&req=5

fig7s1: Remapping with coordinated assemblies.(A) Comparison of single cell phase precession generated bycoordinated assemblies (before and after remapping) and independentcoding. For this simulation, single cell phase and rate fields wereassumed to be perfectly remapped, so that any changes are purely due toassembly interactions. Note that, while assembly interactions improvephase coding in single cells in the initial environment, after remappingthese same interactions disrupt phase precession and cause a lower(circular-linear) correlation between spike phase and animal locationthan that generated by independent cells. (B) Populationfiring rate on a single trial along a linear track. While assemblyinteractions initially entrain and amplify theta oscillations in thepopulation compared to independent cells, after remapping theseinteractions disrupt theta activity and cause a lower overall activitylevel.DOI:http://dx.doi.org/10.7554/eLife.03542.019
Mentions: What are the advantages of independent coding compared to sequence generation throughinteractions between cell assemblies? When an animal is moved between environments,the relative locations at which place cells in CA1 fire remap independently of oneanother (e.g., O'Keefe and Conway,1978; Wilson and McNaughton,1993). This global remapping of spatial representations poses a challenge forgeneration of theta sequences through coordinated assemblies as synaptic interactionsthat promote formation of sequences in one environment would be expected to interferewith sequences in a second environment. Indeed, in the coordinated assembly model,simulations of remapping reduced single cell phase precession to below the level ofindependent cells (i.e., of an identical simulation with interactions between cellsremoved). Remapping in the coordinated coding model also substantially reduced firingrate and population oscillations (Figure7—figure supplement 1). This decrease in firing rate followingremapping contradicts experimental data showing an increase in firing rate in novelenvironments (Karlsson and Frank, 2008). Itis not immediately clear whether the independent coding model faces similarconstraints on sequence generation across different spatial representations. Wetherefore addressed the feasibility of maintaining theta sequences followingremapping given the assumptions that underpin our independent coding model.

Bottom Line: These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies.We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity.Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.

View Article: PubMed Central - PubMed

Affiliation: Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom.

ABSTRACT
Hippocampal place cells encode an animal's past, current, and future location through sequences of action potentials generated within each cycle of the network theta rhythm. These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies. Instead, we find through simulations and analysis of experimental data that rate and phase coding in independent neurons is sufficient to explain the organization of CA1 population activity during theta states. We show that CA1 population activity can be described as an evolving traveling wave that exhibits phase coding, rate coding, spike sequences and that generates an emergent population theta rhythm. We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity. Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.

Show MeSH