Neuron Names: A Gene- and Property-Based Name Format, With Special Reference to Cortical Neurons

Abstract

Precision in neuron names is increasingly needed. We are entering a new era in which classical anatomical criteria are only the beginning toward defining the identity of a neuron as carried in its name. New criteria include patterns of gene expression, membrane properties of channels and receptors, pharmacology of neurotransmitters and neuropeptides, physiological properties of impulse firing, and state-dependent variations in expression of characteristic genes and proteins. These gene and functional properties are increasingly defining neuron types and subtypes. Clarity will therefore be enhanced by conveying as much as possible the genes and properties in the neuron name. Using a tested format of parent-child relations for the region and subregion for naming a neuron, we show how the format can be extended so that these additional properties can become an explicit part of a neuron's identity and name, or archived in a linked properties database. Based on the mouse, examples are provided for neurons in several brain regions as proof of principle, with extension to the complexities of neuron names in the cerebral cortex. The format has dual advantages, of ensuring order in archiving the hundreds of neuron types across all brain regions, as well as facilitating investigation of a given neuron type or given gene or property in the context of all its properties. In particular, we show how the format is extensible to the variety of neuron types and subtypes being revealed by RNA-seq and optogenetics. As current research reveals increasingly complex properties, the proposed approach can facilitate a consensus that goes beyond traditional neuron types.

Keywords: axons; brain regions; dendrites; genomics; neuron classification; terminology.

FIGURE 1

Cross section of the lumbar spinal cord, showing in the ventral horn a principal neuron (alpha motor neuron: MN) with long motor axon to a distant target, a skeletal muscle; and interneurons with short axons that remain within their region of origin.

FIGURE 2

Neostriatum, showing the direct and indirect principal neuron projections to the globus pallidus interna by the medium spiny neurons, and the several types of interneurons, including the large cholinergic interneuron [see text, adapted from Wilson (2004)].

FIGURE 3

Basic pyramidal cell (principal cell) forms the cortical circuit module of three-layer cortex in the turtle dorsal cortex. Red indicates excitatory, blue indicates inhibitory cell. ffexc, feedforward excitatory; fbexc, feedback excitatory; lexc, lateral excitatory; ffinh, feedforward inhibition; fbinh, feedback inhibition [Adapted from Shepherd and Rowe (2017)].

FIGURE 4

Basic pyramidal cell (principal cell) circuit modules of the piriform (olfactory) cortex. Red indicates excitatory neurons, blue indicates inhibitory neurons. SL, semilunar pyramidal cell; sPC, superficial pyramidal cell; dPC, deep pyramidal cell [Adapted from Shepherd and Rowe (2017)].

FIGURE 5

Simplified summary of neurons in the hippocampus, showing the three main subregions: dentate gyrus (DG), CA3, and CA1, with their three main principal neurons: granule cell (Gr), and pyramidal (P) cells in CA3 and CA1. Examples of interneurons are shown for basket (B) cells in dentate gyrus and CA1 [Adapted from NeuronDB: (https://senselab.med.yale.edu/FunctionalConnectomeDB/realisticdiagram/diagram.py?id=154765)].

FIGURE 6

Basic pyramidal cell (principal neuron) types (in red) in the adult neocortex in relation to the six layers and to the three connectivity types: intratelencephalic (IT), pyramidal tract (PT) and corticothalamic (CT). Interneuron examples (in blue) are superficial cells in layer 1, and basket-cell types in relation to pyramidal cell bodies. Red color indicates excitatory neurons, blue indicates inhibitory neurons [Adapted from Shepherd and Rowe (2017)].

FIGURE 7

Relations between firing patterns, laminar localization, connectivity and morphology of pyramidal cells. Types of firing patterns at top are aligned with representative cell morphologies giving the patterns at bottom. Laminar localization is shown (each dot a recorded cell) in the middle separated into IT, PT and CT categories; colors indicate the reconstructed cells at bottom [Adapted from Gouwens et al., 2018].

FIGURE 8

Interneurons (left column) in the neocortex: correlation of expression of calcium-binding proteins (CBPs: middle column: CB, calbindin; PV, parvalbumin; CR, calretinin NPY) and neuropeptides (NPY, neuropeptide Y; VIP, vasoactive intestinal peptide; SOM, somatostatin; CCK, cholecystokinin) with different morphological and electrophysiological classes (right column: AC, accommodating; b, burst; c, classic burst; d, delay burst; iS, irregular spiking; NAC, non-accommodating; STUT, stuttering) [Adapted from Markram et al. (2004)].

FIGURE 9

Summary of steps in neurogenesis and differentiation of the main types of neocortical pyramidal cells based on intracerebral (intratelencephalic IT) and subcerebral (pyramidal tract PT, corticothalamic CT) connectivity, as described in the text. Note the consistency of these types with the adult pyramidal cell types in Figure 3, 4, and 6. [Adapted from Shibata et al. (2015); see also Rakic (2009)].