Spatial memory training induces morphological changes detected by manganese-enhanced MRI in the hippocampal CA3 mossy fiber terminal zone

Hippocampal mossy fibers (MFs) can show plasticity of their axon terminal arbor consequent to learning a spatial memory task. Such plasticity is seen as translaminar sprouting from the stratum lucidum (SL) of CA3 into the stratum pyramidale (SP) and the stratum oriens (SO). However, the functional role of this presynaptic remodeling is still obscure. In vivo imaging that allows longitudinal observation of such remodeling could provide a deeper understanding of this presynaptic growth phenomenon as it occurs over time. Here we used manganese-enhanced magnetic resonance imaging (MEMRI), which shows a high-contrast area that co-localizes with the MFs. This technique was applied in the detection of learning-induced MF plasticity in two strains of rats. Quantitative analysis of a series of sections in the rostral dorsal hippocampus showed increases in the CA3a′ area in MEMRI of trained Wistar rats consistent with the increased SO+SP area seen in the Timm's staining. MF plasticity was not seen in the trained Lister-Hooded rats in either MEMRI or in Timm's staining. This indicates the potential of MEMRI for revealing neuro-architectures and plasticity of the hippocampal MF system in vivo in longitudinal studies. •Translaminar sprouting of hippocampal mossy fiber after learning observed in Wistar but not LH rat.•Consistent change of CA3a area detected by MEMRI compared to swim control.•MEMRI enhancement correlated with Timm's staining of mossy fiber.•We demonstrated the potential of imaging plasticity in neuro-architectures.