Here, we describe a draft mouse brain cell atlas that we created by profiling (using Drop-seq) 690,000 individual cells from nine major regions of the adult mouse brain. By comparing single-cell transcriptional patterns within and across neuron types, we identified and validated a pervasive transcriptional program supporting axon and presynaptic function and discovered large-scale patterns in ion channel gene expression that may enact neurons’ electrophysiological properties. We found that, in the cortex, glutamatergic neurons tend to be specialized by region, while non-neuron cell classes, such as those that make up the vasculature, can be variably specialized across cortical and subcortical areas. We also highlight the neuronal diversity of individual brain regions through the classification of neuron types using examples from the basal ganglia. In the globus pallidus externus (GPe) and substantia nigra reticulata (SNr), where neuron types are not well-understood, we propose complete neuron-type classifications and identify selective markers for each population. In the striatum, where neuronal diversity is well charted, we nonetheless identify a novel group of principal neurons that had been overlooked in decades of research.