Dendritic axon origin enables information gating by perisomatic inhibition in pyramidal neurons

Abstract

Information processing in neuronal networks involves the recruitment of selected neurons into coordinated spatiotemporal activity patterns. This sparse activation results from widespread synaptic inhibition in conjunction with neuron-specific synaptic excitation. We report the selective recruitment of hippocampal pyramidal cells into patterned network activity. During ripple oscillations in awake mice, spiking is much more likely in cells in which the axon originates from a basal dendrite rather than from the soma. High-resolution recordings in vitro and computer modeling indicate that these spikes are elicited by synaptic input to the axon-carrying dendrite and thus escape perisomatic inhibition. Pyramidal cells with somatic axon origin can be activated during ripple oscillations by blocking their somatic inhibition. The recruitment of neurons into active ensembles is thus determined by axonal morphological features.

Cross-strataco-occurrence of ripples with theta-frequency oscillations in the hippocampus of foraging rats

“…Such analyses could also assess the role of neurons with basal dendrites that act as axons during theta vs . non-theta ripples (Hodapp et al, 2022).…”

“…While these are technically challenging experiments, the availability of multielectrode recording probes along with high-resolution voltage imaging and other recording techniques in awake behaving animals make such analyses feasible (Giocomo, 2015;Abdelfattah et al, 2019;Steinmetz et al, 2021;Valero et al, 2022;Zong et al, 2022). Such analyses could also assess the role of neurons with basal dendrites that act as axons during theta vs. non-theta ripples (Hodapp et al, 2022). 0.0012, imm.…”

Function follows form: how the structure of neurons determines cortical network activity

“…While most studies of neuronal signal integration focus on dendrites [ 8 ], more recent work points towards the importance of the axon’s location and properties [ 6 ]. Hodapp and coworkers 4 have now reported a new computational mechanism in cortical networks which is based on the location of the axon. Previous work by the same group had shown that in up to 50% of mouse hippocampal pyramidal cells, the axon emanates from a basal dendrite, rather than from the soma [ 10 ].…”

“…During strong inhibition, the axon-carrying dendrite is the most likely source of excitation for action potential generation. Scale bar, 20 μm (adapted from [ 4 ] …”

“…Progress will depend on close cooperation between cellular and system neurophysiologists, cellular- and network-level neuroanatomists and theoretical neuroscientists. In this respect, the cooperative study conducted by Hodapp and coworkers [ 4 ] is an example for the increasing synergies between different approaches in modern neurosciences: cells and networks, function and form go together in nervous systems, and they must go together in our research.…”