The ventral division of the medial geniculate body (MGV) is the primary tonotopically-organized nucleus of the auditory thalamus. Previous studies have suggested a close association between the anatomical structure of the MGV and its observed functional organization, but direct correlative studies are lacking. In the present study, regional differences in the cytoarchitecture of the rabbit MGV were described. These different regions were shown to have distinct frequency organizations. The central portion of the rabbit MGV is characterized by a laminated cytoarchitecture that is formed from the orderly arrangement of highly-oriented neuronal cell bodies. In this region, there exists a steep frequency gradient that extends across the dorso-ventral axis of the nucleus, orthogonal to the cellular laminae. This frequency gradient is marked by a discontinuous and stepwise-progression of best frequency. In regions lacking a laminated cytoarchitecture, a steep frequency gradient is absent. In addition, the morphology and basic response properties of individual cells were studied with the juxtacellular labeling technique. Two morphological types of projection neurons as well as two types of putative interneurons were identified on the basis of dendritic thickness, cell soma size and spine morphology. Both types of tufted projection neurons had a variety of different response properties, but the Onset pattern and summation response to binaural stimulation predominate. Quantitative spatial analyses demonstrated that the dendritic fields of both types of tufted neurons are highly oriented. Further, for neurons within the laminated portion of the nucleus, the major axis of orientation of the dendritic fields are parallel to the cellular laminae and orthogonal to the frequency gradient. Departures from this orientation parallel changes in Nissl and functional architecture. A model is presented that correlates the discontinuous and step-wise frequency gradient in the nucleus with the size and morphology of dendritic fields. Lastly, three-dimensional reconstructions of anterogradely-labeled thalamocortical axons reveal a novel class of thalamocortical axon that has collaterals to both layer I as well as layers III/IV of primary auditory cortex; these layers were previously thought to have exclusively separate inputs. This novel class of axon is further evidence for multiple parallel channels from the MGV to AI
