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Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition.

Cannon J, Kopell N, Gardner T, Markowitz J - PLoS Comput. Biol. (2015)

Bottom Line: One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activity propagate robustly along a chain of cells connected by highly redundant feedforward excitation.In this model, synchrony and robust timing are maintained not through redundant excitatory connections, but rather through the interaction between the pulse and the spatiotemporal pattern of inhibition that it creates as it circulates the network.These results suggest that spatially and temporally structured inhibition may play a key role in sequence generation.

View Article: PubMed Central - PubMed

Affiliation: Department of Mathematics, Boston University, Boston, Massachusetts, United States of America.

ABSTRACT
Stereotyped sequences of neural activity are thought to underlie reproducible behaviors and cognitive processes ranging from memory recall to arm movement. One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activity propagate robustly along a chain of cells connected by highly redundant feedforward excitation. But recent experimental observations in the avian song production pathway during song generation have shown excitatory activity interacting strongly with the firing patterns of inhibitory neurons, suggesting a process of sequence generation more complex than feedforward excitation. Here we propose a model of sequence generation inspired by these observations in which a pulse travels along a spatially recurrent excitatory chain, passing repeatedly through zones of local feedback inhibition. In this model, synchrony and robust timing are maintained not through redundant excitatory connections, but rather through the interaction between the pulse and the spatiotemporal pattern of inhibition that it creates as it circulates the network. These results suggest that spatially and temporally structured inhibition may play a key role in sequence generation.

No MeSH data available.


A schematic comparing the synfire chain (A) to our proposed model (B).A, The standard synfire chain. Fan-in and fan-out connectivity allows the spike timing of multiple cells in one pool to influence the spike timing of each cell in the next, which ultimately leads to synchronized spiking within pools. B, Parallel chains generate sequences simultaneously with shared feedback inhibition. Cells in each pool share no common excitatory input and do not directly interact with each other. Instead, synchrony is promoted by inhibitory feedback shared by all cells in a pool. When the interneurons are activated repeatedly by spatially recurrent excitatory activity, this common inhibitory input proves sufficient to synchronize spiking within pools (see Fig 2).
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pcbi.1004581.g001: A schematic comparing the synfire chain (A) to our proposed model (B).A, The standard synfire chain. Fan-in and fan-out connectivity allows the spike timing of multiple cells in one pool to influence the spike timing of each cell in the next, which ultimately leads to synchronized spiking within pools. B, Parallel chains generate sequences simultaneously with shared feedback inhibition. Cells in each pool share no common excitatory input and do not directly interact with each other. Instead, synchrony is promoted by inhibitory feedback shared by all cells in a pool. When the interneurons are activated repeatedly by spatially recurrent excitatory activity, this common inhibitory input proves sufficient to synchronize spiking within pools (see Fig 2).

Mentions: A well-studied model that provides a possible answer is the synfire chain [6, 7]. The synfire chain assumes that excitatory (principal) neurons are organized into pools arranged in a redundant feedforward geometry (Fig 1A). Although synfire chains have not been directly observed in HVC, simulations have shown that the redundant synfire geometry combined with a threshold non-linearity can generate stereotyped, precisely timed sequential activity similar to that observed experimentally in HVC.


Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition.

Cannon J, Kopell N, Gardner T, Markowitz J - PLoS Comput. Biol. (2015)

A schematic comparing the synfire chain (A) to our proposed model (B).A, The standard synfire chain. Fan-in and fan-out connectivity allows the spike timing of multiple cells in one pool to influence the spike timing of each cell in the next, which ultimately leads to synchronized spiking within pools. B, Parallel chains generate sequences simultaneously with shared feedback inhibition. Cells in each pool share no common excitatory input and do not directly interact with each other. Instead, synchrony is promoted by inhibitory feedback shared by all cells in a pool. When the interneurons are activated repeatedly by spatially recurrent excitatory activity, this common inhibitory input proves sufficient to synchronize spiking within pools (see Fig 2).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4633124&req=5

pcbi.1004581.g001: A schematic comparing the synfire chain (A) to our proposed model (B).A, The standard synfire chain. Fan-in and fan-out connectivity allows the spike timing of multiple cells in one pool to influence the spike timing of each cell in the next, which ultimately leads to synchronized spiking within pools. B, Parallel chains generate sequences simultaneously with shared feedback inhibition. Cells in each pool share no common excitatory input and do not directly interact with each other. Instead, synchrony is promoted by inhibitory feedback shared by all cells in a pool. When the interneurons are activated repeatedly by spatially recurrent excitatory activity, this common inhibitory input proves sufficient to synchronize spiking within pools (see Fig 2).
Mentions: A well-studied model that provides a possible answer is the synfire chain [6, 7]. The synfire chain assumes that excitatory (principal) neurons are organized into pools arranged in a redundant feedforward geometry (Fig 1A). Although synfire chains have not been directly observed in HVC, simulations have shown that the redundant synfire geometry combined with a threshold non-linearity can generate stereotyped, precisely timed sequential activity similar to that observed experimentally in HVC.

Bottom Line: One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activity propagate robustly along a chain of cells connected by highly redundant feedforward excitation.In this model, synchrony and robust timing are maintained not through redundant excitatory connections, but rather through the interaction between the pulse and the spatiotemporal pattern of inhibition that it creates as it circulates the network.These results suggest that spatially and temporally structured inhibition may play a key role in sequence generation.

View Article: PubMed Central - PubMed

Affiliation: Department of Mathematics, Boston University, Boston, Massachusetts, United States of America.

ABSTRACT
Stereotyped sequences of neural activity are thought to underlie reproducible behaviors and cognitive processes ranging from memory recall to arm movement. One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activity propagate robustly along a chain of cells connected by highly redundant feedforward excitation. But recent experimental observations in the avian song production pathway during song generation have shown excitatory activity interacting strongly with the firing patterns of inhibitory neurons, suggesting a process of sequence generation more complex than feedforward excitation. Here we propose a model of sequence generation inspired by these observations in which a pulse travels along a spatially recurrent excitatory chain, passing repeatedly through zones of local feedback inhibition. In this model, synchrony and robust timing are maintained not through redundant excitatory connections, but rather through the interaction between the pulse and the spatiotemporal pattern of inhibition that it creates as it circulates the network. These results suggest that spatially and temporally structured inhibition may play a key role in sequence generation.

No MeSH data available.