Functional maps within a single neuron

Abstract

The presence and plasticity of dendritic ion channels are well established. However, the literature is divided on what specific roles these dendritic ion channels play in neuronal information processing, and there is no consensus on why neuronal dendrites should express diverse ion channels with different expression profiles. In this review, we present a case for viewing dendritic information processing through the lens of the sensory map literature, where functional gradients within neurons are considered as maps on the neuronal topograph. Under such a framework, drawing analogies from the sensory map literature, we postulate that the formation of intraneuronal functional maps is driven by the twin objectives of efficiently encoding inputs that impinge along different dendritic locations and of retaining homeostasis in the face of changes that are required in the coding process. In arriving at this postulate, we relate intraneuronal map physiology to the vast literature on sensory maps and argue that such a metaphorical association provides a fresh conceptual framework for analyzing and understanding single-neuron information encoding. We also describe instances where the metaphor presents specific directions for research on intraneuronal maps, derived from analogous pursuits in the sensory map literature. We suggest that this perspective offers a thesis for why neurons should express and alter ion channels in their dendrites and provides a framework under which active dendrites could be related to neural coding, learning theory, and homeostasis.

Fig. 1.

Pyramidal neurons express numerous functional maps along the somato-apical trunk. A: typical CA1 pyramidal neuronal morphology (http://www.neuromorpho.org) (Ascoli et al. 2007), depicting the somato apical trunk. Various physiologically relevant measurements vary along the trunk, forming functional maps on local (B) as well as propagating (C) measurements. bAPs, backpropagating action potential; EPSP, excitatory postsynaptic potential.

Fig. 2.

Efficient coding hypothesis from a cellular neurophysiology perspective. A: from a systems neuroscience perspective, neurons in sensory areas efficiently encode natural stimulus statistics corresponding to sensory information in the external world. B: from a cellular neurophysiology perspective, compartments within neurons in different brain regions encode network statistics that are naturally impinging on them, with the network forming the microenvironment where this neuron resides.

Fig. 3.

Non-local influences foster global order from local computations. A: Mexican-hat interactions between adjacent neurons have been postulated to bestow self-organization capabilities on interneuronal sensory maps. B: voltage-gated ion channels influence physiological measurements at adjacent compartments and could bestow self-organization capabilities on intraneuronal sensory maps. G(X; σ) represents a Gaussian function of variable X, with standard deviation σ.