Maturation profile of thalamic neurons responsive to rotational and translational motions

Abstract

Spatial information arising from the canals and otolith organs is processed in vestibular nuclear neurons that are randomly distributed without a clear topography. Topographic representation of the respective inputs was however documented in the inferior olive, a descending relay station. In search of stations that mediate the topographic representation of vestibular inputs, we further examined the thalamus and aimed to investigate the maturation profile of functionally activated vestibular-related thalamic neurons in postnatal rats (P4-P70/adult). Conscious animals were subjected to either horizontal/vertical rotations or linear translations, which are known to activate hair cells of canals and otolith organs, respectively. Neuronal Activated thalamic neurons were detected by immunohistochemistry for Fos expression. Normal stationary and labyrinthectomized controls that were subjected to vestibular stimulations showed sporadically scattered Fos-immunoreactive neurons. During postnatal development, Fos expression evoked by vestibular stimulation was not recognized in the thalamus until P28. Central medial thalamic nucleus (CM), middle paracentral thalamic nucleus (PC) and zone incerta (ZI) showed otolith organ-evoked Fos expression from P28 onwards. Rostral PC and mediodorsal thalamic nucleus (MD) responded to horizontal canal activation from P28 onwards. Subparafascicular thalamic nucleus (SPF) responded to both otolithic and horizontal canal activations by P28. Certain thalamic subnuclei, however, responded only in the adult stage. These included the centrolateral thalamic nuclei (CL) which showed Fos expression with otolithic stimulation whereas the rhomboid thalamic nucleus (Rh) showed Fos expression with stimulation of both the otolith and the horizontal canals. In the adult, MD was the only thalamic subnucleus that responded to otolithic and vertical/horizontal canal stimulations. Taken together, our results document the developmental topography of thalamic subnuclei in recognizing three-dimensional spatial orientation during angular and linear head movements.