Abstract
Clustering of functionally similar synapses in dendrites is thought to affect neuronal input-output transformation by triggering local nonlinearities. However, neither the in vivo impact of synaptic clusters on somatic membrane potential (sVm), nor the rules of cluster formation are elucidated. We develop a computational approach to measure the effect of functional synaptic clusters on sVm response of biophysical model CA1 and L2/3 pyramidal neurons to in vivo-like inputs. We demonstrate that small synaptic clusters appearing with random connectivity do not influence sVm. With structured connectivity, ~10–20 synapses/cluster are optimal for clustering-based tuning via state-dependent mechanisms, but larger selectivity is achieved by 2-fold potentiation of the same synapses. We further show that without nonlinear amplification of the effect of random clusters, action potential-based, global plasticity rules cannot generate functional clustering. Our results suggest that clusters likely form via local synaptic interactions, and have to be moderately large to impact sVm responses.
Highlights
Clustering of functionally similar synapses in dendrites is thought to affect neuronal inputoutput transformation by triggering local nonlinearities
To examine the theoretical conditions of creating functional synaptic clusters via global mechanisms, we first turned to a simplified neuron model equipped with 10 nonlinear subunits, corresponding to idealised dendritic branches (Methods, Fig. 1a) and simulated structural synaptic plasticity in the model
We found that the number of action potentials during individual sharp wave events (Fig. 4c, solid lines) and the amplitude of the somatic depolarisation (Fig. 4e, bright symbols) were insensitive of the arrangement of the synapses into functional clusters, the time spent above dendritic spike threshold in dendritic branches receiving clustered input increased with cluster size (Fig. 4g, bright symbols)
Summary
Clustering of functionally similar synapses in dendrites is thought to affect neuronal inputoutput transformation by triggering local nonlinearities. The spatial scale of the synapses showing correlated activity in vivo has been found to be restricted to ~5–10 μm and involved a small number, ~2–5 dendritic spines[2,4,5,6] This is substantially less than the ~10–20 inputs required to trigger dendritic Na+ or NMDA spikes (characteristic for thin branches) under in vitro conditions[7,8,9,10] leaving the potential impact of the clusters elusive. Global plasticity may strengthen functional synaptic clustering if co-activation of clustered synapses facilitates somatic action potentials that, back-propagating to the dendritic tree, can reinforce these synaptic clusters This global scenario is expected to require the synaptic clusters to control global synaptic plasticity by driving the output of the cell via the amplification of their postsynaptic effect by local dendritic nonlinearities. Using our method we show that, when the connectivity is unstructured, small synaptic clusters do not influence the sVm response of CA1 and
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