Neocortical Axon Arbors Trade-off Material and Conduction Delay Conservation

Abstract

The brain contains a complex network of axons rapidly communicating information between billions of synaptically connected neurons. The morphology of individual axons, therefore, defines the course of information flow within the brain. More than a century ago, Ramón y Cajal proposed that conservation laws to save material (wire) length and limit conduction delay regulate the design of individual axon arbors in cerebral cortex. Yet the spatial and temporal communication costs of single neocortical axons remain undefined. Here, using reconstructions of in vivo labelled excitatory spiny cell and inhibitory basket cell intracortical axons combined with a variety of graph optimization algorithms, we empirically investigated Cajal's conservation laws in cerebral cortex for whole three-dimensional (3D) axon arbors, to our knowledge the first study of its kind. We found intracortical axons were significantly longer than optimal. The temporal cost of cortical axons was also suboptimal though far superior to wire-minimized arbors. We discovered that cortical axon branching appears to promote a low temporal dispersion of axonal latencies and a tight relationship between cortical distance and axonal latency. In addition, inhibitory basket cell axonal latencies may occur within a much narrower temporal window than excitatory spiny cell axons, which may help boost signal detection. Thus, to optimize neuronal network communication we find that a modest excess of axonal wire is traded-off to enhance arbor temporal economy and precision. Our results offer insight into the principles of brain organization and communication in and development of grey matter, where temporal precision is a crucial prerequisite for coincidence detection, synchronization and rapid network oscillations.

Axon Physiology

“…But the role of axonal delays has only been studied in artificial neural networks (87, 271, 344) or in vitro neuronal circuits (33), and additional work will have to be done to describe its implication in hybrid (i.e., neuron-computer) or in in vivo networks. Furthermore, understanding the conflict faced by cortical axons between space (requirement to connect many different postsynaptic neurons) and time (conduction delay that must be minimized) will require further studies (83).…”

Communication and wiring in the cortical connectome

“…Yet a unimodal kernel cannot, for instance, properly portray the spatial clustering of axon terminals observed within the extent of long-range basket and pyramidal cell axon arbors (e.g., Kisvárday et al, 2002; Binzegger et al, 2005, 2007; Budd et al, 2010). Moreover, this approach had to describe separately the apical and basal dendritic trees of the same pyramidal neuron (Snider et al, 2010).…”

Wnt/PCP proteins regulate stereotyped axon branch extension inDrosophila

“…Both imaging and anatomical studies indicate that branching parameters, such as number, length and branch localization points, are also influenced by neuronal type, global branch distribution and connection properties (Stepanyants et al, 2004;Portera-Cailliau et al, 2005;Snider et al, 2010). Recent computational approaches also suggest that Ramon y Cajal's principle of the economic use of wiring space, cytoplasmic material and conduction times are key trade-offs in branch patterning (Budd et al, 2010;Cuntz et al, 2010). Inevitably, all these parameters rely on the very diverse context of function(s) in individual neurons.…”