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Journal Club: Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum (Peng et al., 2017)

Synaptic connectivity in the presubiculum: implications for head-direction circuit topography

During a recent meeting, the Lab discussed a paper titled “Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum” (Peng et al., 2017). It has long been hypothesized that the head-direction signal is maintained by ‘attractor dynamics’. Numerous theoretical models regarding the connectivity of the circuit that would support such properties have been put forward in the relevant literature, yet the experimental demonstration of attractor dynamics remains scarce. In this study, the authors investigate the neuronal microcircuits of the presubiculum, the main recipient of the thalamic inputs that convey the head-direction signal. In particular, they show that the superficial and deep layers have distinct patterns of connectivity. Connections between pyramidal cells (PCs) are almost entirely absent in superficial layers. In contrast, connections among interneurons are high. Furthermore, PC-PC synaptic connection probability in the ventral and dorsal regions of the superficial layers is 0.3% and 0.7% respectively. In sum, the study reveals area-and layer-specific synaptic connectivity in presubiculum, and sets new constraints for future models of the parahippocampal navigation system.

The presubiculum, located between the hippocampus and the entorhinal cortex, plays a fundamental role in representing spatial information, notably head direction (HD). HD cells were first recorded by Jim Ranck in 1984. Neurons of this region are correlated with various aspects of an animal’s location and orientation, and include amongst their ranks HD cells and gird cells. In this 6-layered area, layers I to III are usually referred to as the superficial layers, while layers V and VI are known as deep layers (Tukker et al., 2015). It has been shown that layer III of the presubiculum contains HD cells, and HD cells are also found throughout the layers III, V and VI of the medial entorhinal cortex (MEC) (Boccara et al., 2010). In layer III of the MEC, a clear topography is observed with sharply tuned HD cells present only in the dorsal region (Giocomo et al., 2014). Importantly, layer III of the presubiculum projects primarily to layer III of the MEC in a unidirectional fashion (Preston-Ferrer et al., 2016), and the number of HD cells decreases from the superficial layers to the deep layers in those two areas (Boccara et al., 2010). In addition, the dorsal presubiculum also contains grid cells (Boccara et al., 2010). However, although the presubiculum exhibits a dorsoventral divergence of network topology, the observed layer-specific connectivity exists regardless of the interregional variability. The network topology in the superficial layers of the presubiculum is characterised by the lack of recurrent excitation, indicating that local spatial tuning of PCs here must be generated through interaction with inhibitory cells.

The HD signal is generated subcortically, in the lateral mammillary bodies, and is transmitted by the antero-dorsal nucleus of the thalamus. Cortical feedback, especially from the postsubiculum (PoS), is necessary to anchor the HD signal to the external world. How does this layer specificity of the PoS relate to feedback mechanisms? The feedback projections from PoS to antero-dorsal thalamus and lateral mammillary nuclei originate from PCs in deep layers (Yoder and Taube, 2011). Communication between PCs in superficial layers of the presubiculum can only be achieved through interactions with interneurons, and grid cell activity can be established regardless of the presence or absence of recurrent excitation (Peng et al., 2017). So, it will be important to determine whether the HD cells vary in intrinsic synaptic connectivity, whether the difference in tuning is extrinsic and results from distinct inputs, or whether the different spatially tuned cell types actually belong to disparate subnetworks – each of which is internally consistent and differentially distributed across the dorso-ventral extent of presubiculum (Jeffery, 2014; Peng et al., 2017). The superficial presubiculum represents a suitable network to investigate the mechanisms required for HD cell tuning.

1. Peng Y, Barreda Tomas F J, Klisch C, et al. Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum. Cereb Cortex, 2017, 25: 1-18.
2. Tukker JJ, Tang Q, Burgalossi A, Brecht M. Head-Directional Tuning and Theta Modulation of Anatomically Identified Neurons in the Presubiculum. 2015, J Neurosci, 35(46): 15391-15395.
3. Boccara CN, Sargolini F, Thoresen VH, et al. Grid cells in pre- and parasubiculum. Nat Neurosci, 2010, 13(8): 987-994.
4. Giocomo LM, Stensola T, Bonnevie T, Van Cauter T, Moser MB, Moser EI. Topography of Head Direction Cells in Medial Entorhinal Cortex. Curr Biol, 2014, 24(3): 252-262.
5. Preston-Ferrer P, Coletta S, Frey M, Burgalossi A. Anatomical organization of presubicular head-direction circuits. Elife, 2016, 5.pii: e14592.
6. Yoder RM, Taube JS. Projections to the anterodorsal thalamus and lateral mammillary nuclei arise from different cell populations within the postsubiculum: implications for the control of head direction cells. Hippocampus, 2011, 21(10): 1062-1073.
7. Jeffery K. Spatial mapping: graded precision of entorhinal head direction cells. Curr Bio, 2014, 24(3): R113-114.

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