Optimizing a Neuron for Reliable Dendritic Subunit Pooling

In certain biologically relevant computing scenarios, a neuron "pools" the outputs of multiple independent functional subunits, firing if any one of them crosses threshold. Recent studies suggest that active dendrites could provide the thresholding mechanism, so that both the thresholding and pooling operations could take place within a single neuron. A pooling neuron faces a difficult task, however. Dendrites can produce highly variable responses depending on the density and spatial patterning of their synaptic inputs, and bona fide dendritic firing may be very rare, making it difficult for a neuron to reliably detect when one of its many dendrites has "gone suprathreshold". Our goal has been to identify biological adaptations that optimize a neuron's performance at the binary subunit pooling (BSP) task. Katz et al. (2009) pointed to the importance of spine density gradients in shaping dendritic responses. In a similar vein, we used a compartmental model to study how a neuron's performance at the BSP task is affected by different spine density layouts and other biological variables. We found BSP performance was optimized when dendrites have (1) a decreasing spine density gradient (true for many types of pyramidal neurons); (2) low-to-medium resistance spine necks; (3) strong NMDA currents; (4) fast spiking Na⁺ channels; and (5) powerful hyperpolarizing inhibition. Our findings provide a normative account that links several neuronal properties within the context of a behaviorally relevant task, and may provide new insights into nature's subtle strategies for optimizing the computing capabilities of neural tissue.