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Short-term plasticity constrains spatial organization of a hippocampal presynaptic terminal.

ABSTRACT: Although the CA3-CA1 synapse is critically important for learning and memory, experimental limitations have to date prevented direct determination of the structural features that determine the response plasticity. Specifically, the local calcium influx responsible for vesicular release and short-term synaptic facilitation strongly depends on the distance between the voltage-dependent calcium channels (VDCCs) and the presynaptic active zone. Estimates for this distance range over two orders of magnitude. Here, we use a biophysically detailed computational model of the presynaptic bouton and demonstrate that available experimental data provide sufficient constraints to uniquely reconstruct the presynaptic architecture. We predict that for a typical CA3-CA1 synapse, there are ~70 VDCCs located 300 nm from the active zone. This result is surprising, because structural studies on other synapses in the hippocampus report much tighter spatial coupling. We demonstrate that the unusual structure of this synapse reflects its functional role in short-term plasticity (STP).

SUBMITTER: Nadkarni S

PROVIDER: S-EPMC3437845 | biostudies-other | 2012 Sep

REPOSITORIES: biostudies-other

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Short-term plasticity constrains spatial organization of a hippocampal presynaptic terminal.

Nadkarni Suhita S Bartol Thomas M TM Stevens Charles F CF Sejnowski Terrence J TJ Levine Herbert H

Proceedings of the National Academy of Sciences of the United States of America 20120820 36

Although the CA3-CA1 synapse is critically important for learning and memory, experimental limitations have to date prevented direct determination of the structural features that determine the response plasticity. Specifically, the local calcium influx responsible for vesicular release and short-term synaptic facilitation strongly depends on the distance between the voltage-dependent calcium channels (VDCCs) and the presynaptic active zone. Estimates for this distance range over two orders of ma ...[more]

PMID: 22908295

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Project description:Bottom-up models of functionally relevant patterns of neural activity provide an explicit link between neuronal dynamics and computation. A prime example of functional activity patterns are propagating bursts of place-cell activities called hippocampal replay, which is critical for memory consolidation. The sudden and repeated occurrences of these burst states during ongoing neural activity suggest metastable neural circuit dynamics. As metastability has been attributed to noise and/or slow fatigue mechanisms, we propose a concise mesoscopic model which accounts for both. Crucially, our model is bottom-up: it is analytically derived from the dynamics of finite-size networks of Linear-Nonlinear Poisson neurons with short-term synaptic depression. As such, noise is explicitly linked to stochastic spiking and network size, and fatigue is explicitly linked to synaptic dynamics. To derive the mesoscopic model, we first consider a homogeneous spiking neural network and follow the temporal coarse-graining approach of Gillespie to obtain a "chemical Langevin equation", which can be naturally interpreted as a stochastic neural mass model. The Langevin equation is computationally inexpensive to simulate and enables a thorough study of metastable dynamics in classical setups (population spikes and Up-Down-states dynamics) by means of phase-plane analysis. An extension of the Langevin equation for small network sizes is also presented. The stochastic neural mass model constitutes the basic component of our mesoscopic model for replay. We show that the mesoscopic model faithfully captures the statistical structure of individual replayed trajectories in microscopic simulations and in previously reported experimental data. Moreover, compared to the deterministic Romani-Tsodyks model of place-cell dynamics, it exhibits a higher level of variability regarding order, direction and timing of replayed trajectories, which seems biologically more plausible and could be functionally desirable. This variability is the product of a new dynamical regime where metastability emerges from a complex interplay between finite-size fluctuations and local fatigue.

Dataset Information

Short-term plasticity constrains spatial organization of a hippocampal presynaptic terminal.

Publications

Short-term plasticity constrains spatial organization of a hippocampal presynaptic terminal.

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