The activity of thalamocortical neurons is largely defined by their excitatory inputs. The key determinants of excitatory afferents are the origin, complexity, and density of axon terminals. While some quantitative data are available on these aspects of glutamatergic afferents in animals, organization of excitatory inputs is unknown in the human thalamus. In this study we determined the origin, size and density of glutamatergic axon terminals in the anterior part of the human thalamus, examined their inter- and intra-nuclear heterogeneity as well and s the interindividual variability. We used vGLUT1 and vGLUT2 to label cortical and subcortical excitatory inputs, respectively. Paraventricular thalamic nucleus contained the highest density of, mainly, small vGLUT2+ terminals. Large sized vGLUT2+ terminals were observed in the anteroventral and ventrolateral (VL) nuclei and in patches of variable size and distribution within the mediodorsal nucleus. vGLUT2+ innervation of the ventral anterior nucleus (VA) was sparse, but not absent. Large sized vGLUT1+ terminals were only observed in the caudal part of MD. Neurochemical marker distribution and probabilistic tractography demonstrated that M1 and premotor cortices were preferentially connected to the vGLUT2 rich, calbindin-negative VL (i.e. cerebellar) and vGLUT2 poor, calbindin-positive VA (i.e. basal ganglia recipient) respectively. The position of these motor nuclei differed from the accepted schemes. Our data demonstrate that the size, origin and density of excitatory inputs in the human anterior thalamus display rich variability which indicates nucleus and subnucleus specific integration of incoming information. Mapping glutamatergic afferents allows functional parcellation of this thalamic region.