Morphological and Functional Correlations of Cortical Neural Circuits

Abstract

From the form to the function of the neuron is the ultimate question for cortical neuroscience. Here, we summarize current electrophysiological evidence for correlations between morphology and functional attributes in the primate primary visual cortex (V1) at the level of individual neurons. We highlight three morphological attributes-dendritic arborization, soma size, and synaptic density-and how each maps onto signature functional properties including firing regimes, receptive field structure, and orientation selectivity. Techniques that bridge the range from in vivo multiunit recording (up to the latest Neuropixels probes) to patch-clamp with associated anatomical reconstructions, to two-photon identification of individual neurons, were used to outline the structure-function mappings. Layer 2/3 pyramidal cells with elongated apical dendrites aligned to the cell's orientation preference are more sharply tuned for that orientation, for instance, whereas simple metrics for the circularity of the dendritic field show none of the biases seen with orientation map domain. The PV interneurons are the reverse: highly orientation-selective PV cells are more localized in their dendritic arbors than the broadly tuned cells web.mit.edu. Macaque V1 layer 4 narrow-spiking cells with large somata (and waveform) are highly direction-selective, whereas the other subclass bursts with orientation selectivity. Macaque V1 cells are sparsely innervated synaptically compared to cells at the same laminar location in the mouse (2-5× fewer inputs), indicating species-specific integration that could underlie primate-specific aspects to visual processing. We integrate results from individual layers: layer 4 spiny stellate/pyramidal cells receive profuse thalamic innervations and are likely to be simple field receivers, whereas the larger layer 5 pyramids (with thick tufts, large somata) are the burst-firing cells with broader spatial tuning. Together, these results suggest that the form of the neuron in the V1, dictated by laminar cell type, systematically determines functional output. We derive the implications for cortical circuit models: morphological specializations support independent processing functions, yet orientation tuning is surprisingly robust to perturbations of the dendritic form. The following primate high-resolution imaging-electrophysiology experiments will determine the ultimate human V1 structure-function atlas.