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A direct comparison of afferents to the rat anterior thalamic nuclei and nucleus reuniens: overlapping but different

Mathiasen, ML;Nelson, AJD;Amin, E;O'Mara, SM;Aggleton, JP;

Both nucleus reuniens and the anterior thalamic nuclei are densely interconnected with medial cortical and hippocampal areas, connections that reflect their respective contributions to learning and memory. To better appreciate their comparative roles, pairs of different retrograde tracers were placed in these two thalamic sites in adult rats. Both thalamic sites receive modest cortical inputs from layer V that contrasted with much denser projections from layer VI. Despite frequent overlap in layer VI, ventral prefrontal and anterior cingulate inputs to nucleus reuniens were concentrated in the deepest sublayer (VIb). Meanwhile, inputs to the anterior thalamic nuclei originated more evenly from both sublayers VIa and VIb, with the result that they were often located more superficially than the projections to nucleus reuniens. Again, while the many hippocampal (subiculum) neurons projecting to nucleus reuniens and the anterior thalamic nuclei were partially intermingled within the deep cellular parts of the subiculum, cells projecting to nucleus reuniens consistently tended to lie even deeper, i.e., immediately adjacent to the alveus. Variable numbers of double-labelled cells were present in those cortical and subicular portions where the two cell populations intermingled, though they remained in a minority. Our data also show how projections to these two thalamic sites are organized in opposing dorsal/ventral and rostral/caudal gradients across both the cortex and hippocampal formation. While the anterior thalamic nuclei are preferentially innervated by dorsal cortical sites, more ventral frontal sites preferentially reach nucleus reuniens. These anatomical differences may underpin the complementary cognitive functions of these two thalamic areas.Significance statementBoth nucleus reuniens and the anterior thalamic nuclei link frontal cortical areas with the hippocampal formation. We show that the cortical and hippocampal projections to these thalamic sites show intermingled but opposing gradients of origin across the cerebral cortex (anterior thalamic – more dorsal, nucleus reuniens – more ventral), with their respective afferents typically arising from different neurons. There is also a repeated tendency across cortical areas for nucleus reuniens inputs to arise from the very deepest layer (VIb), while anterior thalamic inputs are often slightly more superficial, located across VIb and VIa. A similar depth distinction is again seen in the subiculum. These patterns indicate a separation of information reaching these two thalamic sites, alongside functional divisions within cortical layer VI.