Abstract
Strings on a violin are tuned to generate distinct sound frequencies in a manner that is firmly dependent on finger location along the fingerboard. Sound frequencies emerging from different violins could be very different based on their architecture, the nature of strings and their tuning. Analogously, active neuronal dendrites, dendrites endowed with active channel conductances, are tuned to distinct input frequencies in a manner that is dependent on the dendritic location of the synaptic inputs. Further, disparate channel expression profiles and differences in morphological characteristics could result in dendrites on different neurons of the same subtype tuned to distinct frequency ranges. Alternately, similar location-dependence along dendritic structures could be achieved through disparate combinations of channel profiles and morphological characteristics, leading to degeneracy in active dendritic spectral tuning. Akin to strings on a violin being tuned to different frequencies than those on a viola or a cello, different neuronal subtypes exhibit distinct channel profiles and disparate morphological characteristics endowing each neuronal subtype with unique location-dependent frequency selectivity. Finally, similar to the tunability of musical instruments to elicit distinct location-dependent sounds, neuronal frequency selectivity and its location-dependence are tunable through activity-dependent plasticity of ion channels and morphology. In this morceau, we explore the origins of neuronal frequency selectivity, and survey the literature on the mechanisms behind the emergence of location-dependence in distinct forms of frequency tuning. As a coda to this composition, we present some future directions for this exciting convergence of biophysical mechanisms that endow a neuron with frequency multiplexing capabilities.
Highlights
The advent of patch clamp electrophysiology allowed direct electrical access to neuronal sub-cellular compartments and paved the way for giant strides in the field of single neuron physiology with a focus on the hitherto unfound active dendritic properties (Stuart et al, 1993)
The focus of this review article is on a specific aspect of dendritic physiology, one that critically relies on active gradients within a dendritic structure and one that endows neurons with location-dependent input processing
The demonstration of location-dependent frequency selectivity mediated by active dendritic conductances (Narayanan and Johnston, 2007, 2008; Hu et al, 2009; Kalmbach et al, 2013; Das and Narayanan, 2014) ushered in the possibility of a novel role for single neurons to detect and synchronize their activity to a frequency of an ongoing network oscillation or perform selective routing of synaptic inputs based on their spectral content (Hong et al, 2007; Buzsáki, 2010; Ratté et al, 2013; Das and Narayanan, 2015)
Summary
The advent of patch clamp electrophysiology allowed direct electrical access to neuronal sub-cellular compartments and paved the way for giant strides in the field of single neuron physiology with a focus on the hitherto unfound active dendritic properties (Stuart et al, 1993). Juxtaposed with the literature on inhomogeneous distribution of dendritic conductances, spatiotemporal interactions between them, plasticity of intrinsic neuronal properties, activity- and state-dependent modulation of expression profiles and degeneracy in neuronal physiology, we can posit a complex yet nuanced role for plastic active dendrites in spectral tuning of single neurons. The aim of this narrative is to discuss the various forms and mechanisms of spectral tuning present in neurons with the focus primarily on the role of dendrites. We highlight the several endeavors undertaken to dissect various forms of neuronal spectral tuning, deliberate over their implications for dendritic physiology and eventually propose tenable future directions for steering research in this field
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