Many brain structures project to both the anteroventral thalamic nucleus and the anteromedial thalamic nucleus. In the present study, pairs of different tracers were placed into these two thalamic sites in the same rats to determine the extent to which these nuclei receive segregated inputs. Only inputs from the laterodorsal tegmental nucleus, the principal extrinsic cholinergic source for these thalamic nuclei, showed a marked degree of collateralization, with approximately 13% of all cells labeled in this tegmental area projecting to both nuclei. Elsewhere, double-labeled cells were very scarce, making up ∼1% of all labeled cells. Three general patterns of anterior thalamic innervation were detected in these other areas. In some sites, e.g., prelimbic cortex, anterior cingulate cortex, and secondary motor area, cells projecting to the anteromedial and anteroventral thalamic nuclei were closely intermingled, with often only subtle distribution differences. These same projections were also often intermingled with inputs to the mediodorsal thalamic nucleus, but again there was little or no collateralization. In other sites, e.g., the subiculum and retrosplenial cortex, there was often less overlap of cells projecting to the two anterior thalamic nuclei. A third pattern related to the dense inputs from the medial mammillary nucleus, where well-defined topographies ensured little intermingling of the neurons that innervate the two thalamic nuclei. The finding that a very small minority of cortical and limbic inputs bifurcates to innervate both anterior thalamic nuclei highlights the potential for parallel information streams to control their functions, despite arising from common regions. J. Comp. Neurol. 521: 2966–2986, 2013. © 2013 Wiley Periodicals, Inc.