Topological organization of CA3‐to‐CA1 excitation

Abstract

The CA1-projecting axons of CA3 pyramidal cells, called Schaffer collaterals, constitute one of the major information flow routes in the hippocampal formation. Recent anatomical studies have revealed the non-random structural connectivity between CA3 and CA1, but little is known regarding the functional connectivity (i.e. how CA3 network activity is functionally transmitted downstream to the CA1 network). Using functional multi-neuron calcium imaging of rat hippocampal slices, we monitored the spatiotemporal patterns of spontaneous CA3 and CA1 burst activity under pharmacological GABAergic blockade. We found that spatially clustered CA3 activity patterns were transformed into layered CA1 activity sequences. Specifically, synchronized bursts initiated from multiple hot spots in CA3 ensembles, and CA1 neurons located deeper in the pyramidal cell layer were recruited during earlier phases of the burst events. The order of these sequential activations was maintained across the bursts, but the sequence velocity varied depending on the inter-burst intervals. Thus, CA3 axons innervate CA1 neurons in a highly topographical fashion.

Taxonomic Separation of Hippocampal Networks: Principal Cell Populations and Adult Neurogenesis

“…As pointed out by Schultz and Rolls ( 1999 ), these relations would allow CA3 cells to serve not only one but multiple segregated information streams. Quantitative observations relate well to the recent definition of subsets of CA1 pyramidal cells based on overlapping cytoarchitectural, neurochemical, and connectional criteria (Deguchi et al, 2011 ; Slomianka et al, 2011 ; Lee et al, 2014 ), physiological characteristics (Mizuseki et al, 2011 ; Hongo et al, 2015 ; Valero et al, 2015 ) and gene-expression data (Thompson et al, 2008 ; Dong et al, 2009 ; Zeisel et al, 2015 ). In the non-rodent CA1, quantitative relations would allow streams to be represented by non-overlapping cell populations that each can be served by the entire CA3 population.…”

Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit

“…Anatomical constraints of the connectivity were implemented in the model by accounting for the distribution of the axonal boutons as a function of longitudinal and transverse distance from the presynaptic cell soma ( Figure 1—figure supplement 2 ). The afferent divergence and convergence onto the cells were also anatomically patterned, maintaining the topographical arrangement seen experimentally ( Hongo et al, 2015 ), for a total of 5.19 billion synaptic connections in the model network. In addition, the remaining parameters that could not be constrained by experimental data were documented, with the assumptions used to arrive at them explicitly listed in Table 2 of Bezaire and Soltesz (2013) and additional parameter calculations described in the Appendix of the present paper, section 'Inhibitory connectivity'.…”

Place cells are more strongly tied to landmarks in deep than in superficial CA1

“…And along the radial axis of CA1 pyramidal layer, the deep layer (CA1d, bordering oriens) receives about 2.5 times more CA2 inputs than the superficial layer (CA1s, bordering radiatum) 22 . This comes in addition to differences in local circuits, molecular expression 23 and physiological properties, with notably CA1d and CA1s pyramidal cells showing differences in number of place fields, bursting activity, spike phase relationship with theta/gamma oscillations 24 , reward influence 25 and firing activity during ripples oscillations 26 27 . Second, CA1 intrinsic connectivity is well suited for functional division, compared with CA3 for instance.…”