Anatomical and functional connectomes underlying hierarchical visual processing in mouse visual system.

Over the last 10 years, there has been a surge in interest in the rodent visual system resulting from the discovery of visual processing functions shared with primates V1, and of a complex anatomical structure in the extrastriate visual cortex. This surprisingly intricate visual system was elucidated by recent investigations using rapidly growing genetic tools primarily available in the mouse. Here, we examine the structural and functional connections of visual areas that have been identified in mice mostly during the past decade, and the impact of these findings on our understanding of brain functions associated with vision. Special attention is paid to structure-function relationships arising from the hierarchical organization, which is a prominent feature of the primate visual system. Recent evidence supports the existence of a hierarchical organization in rodents that contains levels that are poorly resolved relative to those observed in primates. This shallowness of the hierarchy indicates that the mouse visual system incorporates abundant non-hierarchical processing. Thus, the mouse visual system provides a unique opportunity to study non-hierarchical processing and its relation to hierarchical processing.

Architectonic features and relative locations of primary sensory and related areas of neocortex in mouse lemurs.

Mouse lemurs are the smallest of the living primates, and are members of the understudied radiation of strepsirrhine lemurs of Madagascar. They are thought to closely resemble the ancestral primates that gave rise to present day primates. Here we have used multiple histological and immunochemical methods to identify and characterize sensory areas of neocortex in four brains of adult lemurs obtained from a licensed breeding colony. We describe the laminar features for the primary visual area (V1), the secondary visual area (V2), the middle temporal visual area (MT) and area prostriata, somatosensory areas S1(3b), 3a, and area 1, the primary motor cortex (M1), and the primary auditory cortex (A1). V1 has "blobs" with "nonblob" surrounds, providing further evidence that this type of modular organization might have evolved early in the primate lineage to be retained in all extant primates. The laminar organization of V1 further supports the view that sublayers of layer 3 of primates have been commonly misidentified as sublayers of layer 4. S1 (area 3b) is proportionately wider than the elongated area observed in anthropoid primates, and has disruptions that may distinguish representations of the hand, face, teeth, and tongue. Primary auditory cortex is located in the upper temporal cortex and may include a rostral area, R, in addition to A1. The resulting architectonic maps of cortical areas in mouse lemurs can usefully guide future studies of cortical connectivity and function.

The Mouse Cortical Connectome, Characterized by an Ultra-Dense Cortical Graph, Maintains Specificity by Distinct Connectivity Profiles.

The inter-areal wiring pattern of the mouse cerebral cortex was analyzed in relation to a refined parcellation of cortical areas. Twenty-seven retrograde tracer injections were made in 19 areas of a 47-area parcellation of the mouse neocortex. Flat mounts of the cortex and multiple histological markers enabled detailed counts of labeled neurons in individual areas. The observed log-normal distribution of connection weights to each cortical area spans 5 orders of magnitude and reveals a distinct connectivity profile for each area, analogous to that observed in macaques. The cortical network has a density of 97%, considerably higher than the 66% density reported in macaques. A weighted graph analysis reveals a similar global efficiency but weaker spatial clustering compared with that reported in macaques. The consistency, precision of the connectivity profile, density, and weighted graph analysis of the present data differ significantly from those obtained in earlier studies in the mouse.

Modularity in the Organization of Mouse Primary Visual Cortex.

Layer 1 (L1) of primary visual cortex (V1) is the target of projections from many brain regions outside of V1. We found that inputs to the non-columnar mouse V1 from the dorsal lateral geniculate nucleus and feedback projections from multiple higher cortical areas to L1 are patchy. The patches are matched to a pattern of M2 muscarinic acetylcholine receptor expression at fixed locations of mouse, rat, and monkey V1. Neurons in L2/3 aligned with M2-rich patches have high spatial acuity, whereas cells in M2-poor zones exhibited high temporal acuity. Together M2+ and M2- zones form constant-size domains that are repeated across V1. Domains map subregions of the receptive field, such that multiple copies are contained within the point image. The results suggest that the modular network in mouse V1 selects spatiotemporally distinct clusters of neurons within the point image for top-down control and differential routing of inputs to cortical streams.