Synapse Distribution Suggests a Two-Stage Model of Dendritic Integration in CA1 Pyramidal Neurons

Katz, Yael; Menon, Vilas; Nicholson, Daniel A.; Geinisman, Yuri; Kath, William L.; Spruston, Nelson

doi:10.1016/j.neuron.2009.06.023

Cited by 161 publications

(201 citation statements)

References 32 publications

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“…Given the importance of branchspecific NMDA spikes in LTP induction, differential strength of synapses along oblique dendrites may allow synapses along the branch to have an equivalent role in triggering LTP and, secondarily, influencing somatic voltage [43]. These results underscore another goal that synapses must accomplish: adjusting synapses at different locations to allow them to have equal influence on processes that depend on the cooperative action of synapses.…”

Section: (D) Long-term Depressionmentioning

confidence: 96%

Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling

Lisman

2017

Phil. Trans. R. Soc. B

139

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Synapses are complex because they perform multiple functions, including at least six mechanistically different forms of plasticity. Here, I comment on recent developments regarding these processes. (i) Short-term potentiation (STP), a Hebbian processthat requires small amounts of synaptic input, appearsto make strong contributions to some forms of working memory. (ii) The rules for long-term potentiation (LTP) induction in CA3 have been clarified: induction does not depend obligatorily on backpropagating sodium spikes but, rather, on dendritic branch-specific N-methyl-D-aspartate (NMDA) spikes. (iii) Late LTP, a process that requires a dopamine signal (and is therefore neoHebbian), is mediated by trans-synaptic growth of the synapse, a growth that occurs about an hour after LTP induction. (iv) LTD processes are complex and include both homosynaptic and heterosynaptic forms. (v) Synaptic scaling produced by changes in activity levels are not primarily cell-autonomous, but rather depend on network activity. (vi) The evidence for distance-dependent scaling along the primary dendrite is firm, and a plausible structural-based mechanism is suggested.Ideas about the mechanisms of synaptic function need to take into consideration newly emerging data about synaptic structure. Recent superresolution studies indicate that glutamatergic synapses are modular (module size 70 -80 nm), as predicted by theoretical work. Modules are trans-synaptic structures and have high concentrations of postsynaptic density-95 (PSD-95) and a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor. These modules function as quasi-independent loci of AMPA-mediated transmission and may be independently modifiable, suggesting a new understanding of quantal transmission.This article is part of the themed issue 'Integrating Hebbian and homeostatic plasticity.'

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Section: (D) Long-term Depressionmentioning

confidence: 96%

Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling

Lisman

2017

Phil. Trans. R. Soc. B

139

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“…There is substantial evidence that the size of a spine provides information about the efficacy of the synapse that resides on it: the volume of a spine is proportional to (1) the number of vesicles in the presynaptic terminal (Harris and Stevens, 1989); (2) the area of the postsynaptic density (Harris and Stevens, 1989;Knott et al, 2006;Arellano et al, 2007;Katz et al, 2009); (3) the number of postsynaptic AMPA receptors (Katz et al, 2009); and (4) the amplitude of the EPSC measured in the postsynaptic neuron following uncaging of glutamate near the spine (Matsuzaki et al, 2001). Furthermore, long-term potentiation of synapses is associated with an increase in the volume of spines (Matsuzaki et al, 2004;Kopec et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Multiplicative Dynamics Underlie the Emergence of the Log-Normal Distribution of Spine Sizes in the Neocortex In Vivo

Loewenstein¹,

Kuras²,

Rumpel³

2011

Journal of Neuroscience

232

286

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What fundamental properties of synaptic connectivity in the neocortex stem from the ongoing dynamics of synaptic changes? In this study, we seek to find the rules shaping the stationary distribution of synaptic efficacies in the cortex. To address this question, we combined chronic imaging of hundreds of spines in the auditory cortex of mice in vivo over weeks with modeling techniques to quantitatively study the dynamics of spines, the morphological correlates of excitatory synapses in the neocortex. We found that the stationary distribution of spine sizes of individual neurons can be exceptionally well described by a log-normal function. We furthermore show that spines exhibit substantial volatility in their sizes at timescales that range from days to months. Interestingly, the magnitude of changes in spine sizes is proportional to the size of the spine. Such multiplicative dynamics are in contrast with conventional models of synaptic plasticity, learning, and memory, which typically assume additive dynamics. Moreover, we show that the ongoing dynamics of spine sizes can be captured by a simple phenomenological model that operates at two timescales of days and months. This model converges to a log-normal distribution, bridging the gap between synaptic dynamics and the stationary distribution of synaptic efficacies.

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“…This phenomenon has been earlier explored from a theoretical perspective in a passive model of a dendritic tree [28]. Recent experimental and computational studies of Katz et al [39] show that the synapses are scaled in the direction of normalising the contribution of individual inputs to dendritic spikes in CA1 pyramidal neurons. It would be useful to extend [28] and investigate democracy in the presence of active conductances within the framework we have presented here.…”

Section: Discussionmentioning

confidence: 98%

Travelling waves in a model of quasi-active dendrites with active spines

Timofeeva

2010

Physica D: Nonlinear Phenomena

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Synapse Distribution Suggests a Two-Stage Model of Dendritic Integration in CA1 Pyramidal Neurons

Cited by 161 publications

References 32 publications

Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling

Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling

Multiplicative Dynamics Underlie the Emergence of the Log-Normal Distribution of Spine Sizes in the Neocortex In Vivo

Travelling waves in a model of quasi-active dendrites with active spines

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