Angular tuning bias of vibrissa-responsive cells in the paralemniscal pathway

One of the most salient features of primary vibrissal afferents is their sensitivity to the direction in which the vibrissae move. Directional sensitivity is also well conserved in brainstem, thalamic, and cortical neurons of the lemniscal pathway, indicating that this property plays a key role in the organization of the vibrissal system. Here, we show that directional tuning is also a fundamental feature of second-order interpolaris neurons that give rise to the paralemniscal pathway. Quantitative assessment of responses to vibrissa deflection revealed an anisotropic organization of receptive fields with regard to topography, response magnitude, and the degree of angular tuning. Responses evoked by all vibrissae within the receptive field of each cell exhibited a high consistency of direction preference, but a striking difference in angular tuning preference was found among cells that reside in the rostral and caudal divisions of the interpolaris nucleus. Although in caudal interpolaris vectors of angular preference pointed in all directions, in rostral interpolaris virtually all vectors pointed upward, revealing a strong preference for this direction. Control experiments showed that the upward bias did not rely on a preferential innervation of rostral cells by upwardly tuned primary vibrissa afferents, nor did it rely on a direction-selective recruitment of feedforward inhibition. We thus propose that the upward preference bias of rostral cells, which project to the posterior group of the thalamus, emerges from use-dependent synaptic processes that relate to the kinematics of whisking.