Abstract
We investigated the synaptic innervation of apical dendrites of cortical pyramidal cells in a region between layers (L) 1 and 2 using 3-D electron microscopy applied to four cortical regions in mouse. We found the relative inhibitory input at the apical dendrite's main bifurcation to be more than 2-fold larger for L2 than L3 and L5 thick-tufted pyramidal cells. Towards the distal tuft dendrites in upper L1, the relative inhibitory input was at least about 2-fold larger for L5 pyramidal cells than for all others. Only L3 pyramidal cells showed homogeneous inhibitory input fraction. The inhibitory-to-excitatory synaptic ratio is thus specific for the types of pyramidal cells. Inhibitory axons preferentially innervated either L2 or L3/5 apical dendrites, but not both. These findings describe connectomic principles for the control of pyramidal cells at their apical dendrites and support differential computational properties of L2, L3 and subtypes of L5 pyramidal cells in cortex.
Highlights
The image volumes were located at the border of layers 1 and 2, the site of the main bifurcation of apical dendrites from almost all pyramidal neurons of layers 2 to 5 (Figure 1a,b)
To determine the layer origin of each apical dendrite (AD), we first identified those ADs with a soma in the image volume as layer 2 (L2) ADs, and the remaining ADs as ‘deeper layer’ (DL ADs), Karimi et al eLife 2020;9:e46876
The preference of axons to either innervate shafts or spines of ADs was almost binary (Figure 2b): 91 of 92 axons seeded from the shafts of L2 ADs made at least 80% of their other output synapses again onto shafts
Summary
The apical dendrites of pyramidal neurons, the most abundant cell type in the mammalian cerebral cortex (Cajal, 1899; DeFelipe and Farinas, 1992), have been a key focus of anatomical (Cajal, 1899), electrophysiological (Stuart and Sakmann, 1994; Larkum et al, 1999) and in-vivo functional studies (Svoboda et al, 1997; Letzkus et al, 2011; Takahashi et al, 2016). Of particular interest has been the coupling of long-range top-down inputs converging at the apical tufts in layer 1 with synaptic inputs on the basal dendrites in large layer 5 pyramidal cells (Larkum et al, 1999; Larkum, 2013). Understanding the innervation profile of synaptic input onto apical dendrites in this peculiar part of the mammalian cerebral cortex was the goal of this study
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