Abstract
Synaptic transmission, connectivity, and dendritic morphology mature in parallel during brain development and are often disrupted in neurodevelopmental disorders. Yet how these changes influence the neuronal computations necessary for normal brain function are not well understood. To identify cellular mechanisms underlying the maturation of synaptic integration in interneurons, we combined patch-clamp recordings of excitatory inputs in mouse cerebellar stellate cells (SCs), three-dimensional reconstruction of SC morphology with excitatory synapse location, and biophysical modeling. We found that postnatal maturation of postsynaptic strength was homogeneously reduced along the somatodendritic axis, but dendritic integration was always sublinear. However, dendritic branching increased without changes in synapse density, leading to a substantial gain in distal inputs. Thus, changes in synapse distribution, rather than dendrite cable properties, are the dominant mechanism underlying the maturation of neuronal computation. These mechanisms favor the emergence of a spatially compartmentalized two-stage integration model promoting location-dependent integration within dendritic subunits.
Highlights
Dendritic integration of spatio-temporal synaptic activity is fundamental to neuronal computation, which shapes the transformation of input activity into output spiking (Silver, 2010)
Unlike unitary inputs in other neuron types, we found that adult stellate cells (SCs) had smaller and slower miniature excitatory postsynaptic currents than those observed in immature SCs
These conductance changes are locally integrated within dendrites into excitatory postsynaptic potentials (EPSPs), which propagate to the soma where they contribute to somatic voltage
Summary
Dendritic integration of spatio-temporal synaptic activity is fundamental to neuronal computation, which shapes the transformation of input activity into output spiking (Silver, 2010). The maturation of neuronal excitability and morphology (Cathala et al, 2003; Cline, 2016; McCormick and Prince, 1987; Zhang, 2004) is associated with restriction of neuronal connectivity to subcellular compartments (Ango et al, 2004), activity-dependent synaptic rearrangement (Chen and Regehr, 2000; Cline, 2016; Kwon and Sabatini, 2011; Li et al, 2011) and the maturation of excitatory (Cathala et al, 2003; Hestrin, 1992; Koike-Tani et al, 2005; Lawrence and Trussell, 2000; Taschenberger and von Gersdorff, 2000) and inhibitory synaptic inputs (Ben-Ari, 2002; Sanes, 1993; Tia et al, 1996) Despite this knowledge, how developmental changes in cellular parameters dictate dendritic operations and their associated neuronal computations, remains largely unexplored
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