Anatomical and molecular characterization of dopamine D1 receptor-expressing neurons of the mouse CA1 dorsal hippocampus

Abstract

In the hippocampus, a functional role of dopamine D1 receptors (D1R) in synaptic plasticity and memory processes has been suggested by electrophysiological and pharmacological studies. However, comprehension of their function remains elusive due to the lack of knowledge on the precise localization of D1R expression among the diversity of interneuron populations. Using BAC transgenic mice expressing enhanced green fluorescent protein under the control of D1R promoter, we examined the molecular identity of D1R-containing neurons within the CA1 subfield of the dorsal hippocampus. In agreement with previous findings, our analysis revealed that these neurons are essentially GABAergic interneurons, which express several neurochemical markers, including calcium-binding proteins, neuropeptides, and receptors among others. Finally, by using different tools comprising cell type-specific isolation of mRNAs bound to tagged-ribosomes, we provide solid data indicating that D1R is present in a large proportion of interneurons expressing dopamine D2 receptors. Altogether, our study indicates that D1Rs are expressed by different classes of interneurons in all layers examined and not by pyramidal cells, suggesting that CA1 D1R mostly acts via modulation of GABAergic interneurons.Electronic supplementary materialThe online version of this article (doi:10.1007/s00429-016-1314-x) contains supplementary material, which is available to authorized users.

Specific hippocampal interneurons shape consolidation of recognition memory

“…As described (Marsicano and Lutz, 1999), detectable levels of CB 1 receptor mRNA were present throughout the hippocampus both in pyramidal neurons and in GABAergic interneurons (Figure S2C). The distribution of mCherry-tagged D 1positive neurons in the dorsal CA1 region of D 1 -CRE mice was similar to previously published data (Puighermanal et al, 2017, Gangarossa et al, 2012.…”

“…Therefore, our data reveal a specific function of a novel class of CB 1 -and D 1positive interneurons (Puighermanal et al, 2017).…”

“…This suggests that CB 1 receptors in striatal D 1 -positive cells do not participate to this type of memory. Anatomical data indicate that a subset of hippocampal neurons contain D 1 receptors (Gangarossa et al, 2012), likely co-expressing CB 1 protein (Puighermanal et al, 2017). As the hippocampus is a key region for memory, we used the same strategy as described above, to re-express the CB 1 gene in the hippocampus of D 1 -CB 1 -KO mice to obtain HPC-CB 1 -RS mice (Figure 1D,G).…”

“…For instance, the exposure to hippocampal-dependent behavioral tasks induces changes in long-term potentiation (LTP) of synaptic transmission that require the activation of D 1 -like receptors (Frey et al, 1990, Granado et al, 2008, Li et al, 2003, Lemon and Manahan-Vaughan, 2006. Recently, it has been shown that a subclass of hippocampal CCK-positive interneurons, which express CB 1 receptors, contains dopamine D 1 receptors, thus potentially representing a novel subpopulation of CB 1 expressing hippocampal interneurons (Puighermanal et al, 2017, Gangarossa et al, 2012. However, the potential interactions between D 1 and CB 1 receptors in regulating learning-induced plasticity, activity of hippocampal inhibitory circuits and memory processes remain unexplored.…”

Repeated Exposure to D-Amphetamine Decreases Global Protein Synthesis and Regulates the Translation of a Subset of mRNAs in the Striatum

“…Resulting cDNA was used for quantitative real-time PCR (qRT-PCR), using 2X SYBR Green Mix and LC480 Real-Time PCR System (Roche) as described (Puighermanal et al, 2016b). Analysis was performed using LightCycler ® 480 Software (Roche).…”