Electrical Compartmentalization in Neurons

Abstract

Graphical AbstractHighlights d Neural computation relies on compartmentalized dendrites to discern inputs d A method is described to systematically derive the degree of compartmentalization d There are substantially fewer functional compartments than dendritic branches d Compartmentalization is dynamic and can be tuned by synaptic inputs In BriefMany neuronal computations rely on the compartmentalization of dendrites into functional subunits. Wybo et al. investigate the number of these subunits that can coexist on a neuron. They find that there are substantially fewer subunits than dendritic branches but that subunit extent and number can be modified by synaptic inputs. SUMMARYThe dendritic tree of neurons plays an important role in information processing in the brain. While it is thought that dendrites require independent subunits to perform most of their computations, it is still not understood how they compartmentalize into functional subunits. Here, we show how these subunits can be deduced from the properties of dendrites. We devised a formalism that links the dendritic arborization to an impedance-based tree graph and show how the topology of this graph reveals independent subunits. This analysis reveals that cooperativity between synapses decreases slowly with increasing electrical separation and thus that few independent subunits coexist. We nevertheless find that balanced inputs or shunting inhibition can modify this topology and increase the number and size of the subunits in a context-dependent manner. We also find that this dynamic recompartmentalization can enable branch-specific learning of stimulus features. Analysis of dendritic patch-clamp recording experiments confirmed our theoretical predictions.

The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

“…The fine-scale functional organization of the presynaptic circuitry implies that DSGCs may be capable of highly parallel processing of motion information. Modeling studies suggest that nonlinear integration can occur independently in highly branched dendritic structures (Koch et al, 1982;Rall, 1964;Wybo et al, 2019). Moreover, local inhibitory input dramatically increase the ability of neighboring sites to function as independent units (Wybo et al, 2019), as we have observed for DSGCs.…”

“…Modeling studies suggest that nonlinear integration can occur independently in highly branched dendritic structures (Koch et al, 1982;Rall, 1964;Wybo et al, 2019). Moreover, local inhibitory input dramatically increase the ability of neighboring sites to function as independent units (Wybo et al, 2019), as we have observed for DSGCs. Although our data cannot speak to whether each site is independently 'integrating' synaptic input in the sense of triggering a Na + spike, we can say that direction-selective information is present at each site, which could certainly support local spike generation with high directional accuracy.…”

“…It is important to note that nonlinearities inherent in the dendritic Ca 2+ -permeable channels are expected to produce signals that are more compartmentalized than the underlying local dendritic voltage (Wybo et al, 2019;Meier and Borst, 2019;Grimes et al, 2010; Figure 7). Interestingly, Ca 2+ responses remained confined to small sections of the dendrite over several hundred milliseconds, indicative of the strong buffering mechanisms dendrites (Biess et al, 2011;Awatramani et al, 2007).…”

“…Synaptically-evoked Ca 2+ signals are expected to be more compartmentalized than dendritic voltage (Wybo et al, 2019;Meier and Borst, 2019;Grimes et al, 2010), since they arise from inherently nonlinear sources (voltage-gated channels and NMDA receptors). Such nonlinearities are also expected to promote the apparent independence of dendritic activity (Grimes et al, 2010), and could explain how nearby dendritic regions could express different directional tuning properties.…”

Actin remodeling, the synaptic tag and the maintenance of synaptic plasticity

“…[50][51][52][53] Analysis of voltage spread shows a strong attenuation of voltage at dendritic branch-points, supporting the view of an electric dendritic compartment. 54 Dendrites contain ionic conductances capable of generating non-linear active dendritic events-dendritic spikes-in response to local synaptic activity, placing dendrites as the integration unit. Dendritic activated glutamate receptors and voltage-gated calcium and sodium channels can be activated by synchronous activation of spatially clustered synapses generating electric fields that propagate along the entire dendritic branch.…”