Analysis of feedforward mechanisms of multiwhisker receptive field generation in a model of the rat barrel cortex.

There is substantial anatomical segregation in the organization of the rodent barrel system - each whisker on the mystacial pad sends input to TC cells within a dedicated thalamic barreloid, which in turn innervates a corresponding cortical barrel, and RS cells within a barrel respond primarily to deflections of the corresponding whisker at the beginning of the dedicated transmission line (the principal whisker, PW). However, it is also well-established that barrel cells exhibit multiwhisker receptive fields (RFs), and display lower amplitude, longer latency responses to deflections of non-PWs (or adjacent whiskers, AWs). There is considerable controversy regarding the origin of such multiwhisker RFs; three possibilities include: (i) TC cells within a barreloid respond to multiple whiskers, and barrel RS cells simply inherit multiwhisker responses from their aligned barreloid; (ii) TC cells respond only to the PW, but individual barreloids innervate multiple barrels; (iii) multiwhisker responses of barrel cells arise from lateral corticocortical (barrel-to-barrel) synaptic transmission. Ablation studies attempting to pinpoint the source of RS cell AW responses are often contradictory (though experimental work tends to suggest possibilities (i) or (iii) to be most plausible), and hence it is important to carefully evaluate these hypotheses in terms of available physiological data on barreloid and barrel response dynamics. In this work, I employ a biologically detailed model of the rat barrel cortex to evaluate possibility (i), and I show that, within the model, hypothesis (i) is capable of explaining a broad range of the available physiological data on responses to single (PW or AW) deflections and paired whisker deflections (AW deflection followed by PW deflection), as well as the dependence of such responses on the angular direction of whisker deflection. In particular, the model shows that barrel RS cells can exhibit AW direction tuning despite the fact that barreloid to barrel wiring has no systematic dependence on the AW direction preference of TC cells. Future modeling work will examine the other possibilities for the generation of multiwhisker RS cell RFs, and compare and contrast the different possible mechanisms within the context of available experimental data.