Abstract
Conscious memories are critically dependent upon bilateral hippocampal formation, and interhemispheric commissural projections made by mossy cells and CA3 pyramidal cells. GABAergic interneurons also make long-range axonal projections, but little is known regarding their commissural, inter-hippocampal connections. We used retrograde and adeno-associated viral tracing, immunofluorescence and electron microscopy, and in vitro optogenetics to assess contralateral projections of neurochemically defined interneuron classes. We found that contralateral-projecting interneurons were 24-fold less common compared to hilar mossy cells, and mostly consisted of somatostatin- and parvalbumin-expressing types. Somatostatin-expressing cells made denser contralateral axonal projections than parvalbumin-expressing cells, although this was typically 10-fold less than the ipsilateral projection density. Somatostatin-expressing cells displayed a topographic-like innervation according to the location of their somata, whereas parvalbumin-expressing cells mostly innervated CA1. In the dentate gyrus molecular layer, commissural interneuron post-synaptic targets were predominantly putative granule cell apical dendrites. In the hilus, varicosities in close vicinity to various interneuron subtypes, as well as mossy cells, were observed, but most contralateral axon varicosities had no adjacent immunolabeled structure. Due to the relative sparsity of the connection and the likely distal dendritic location of their synapses, commissural projections made by interneurons were found to be weak. We postulate that these projections may become functionally active upon intense network activity during tasks requiring increased memory processing.
Highlights
The hippocampus plays a key role in learning and memory of contexts and events
We show that genetically defined SOMIs in the dentate gyrus (DG)-hilus, CA3 and CA1 hippocampal regions make topographic axonal projections to granule cells (GCs), GABAergic cell and mossy cell targets in the contralateral hippocampus, and predominantly target their distal dendrites
We numerically quantify these connections in terms of projecting cell numbers and the density of their axonal ramification in each region of the hippocampus, and show that these axons have a mean density of ∼10% of their ipsilateral counterparts
Summary
The hippocampus plays a key role in learning and memory of contexts and events. Information is processed via the classical canonical tri-synaptic path comprising the dentate gyrus (DG) as the input gate of the hippocampus, in which information is encoded by granule cells (GCs) and transmitted via their ‘mossy fibers’ to CA3 pyramidal cells (PCs), and from there via Schaffer collaterals to CA1 PCs. Similar to these strong glutamatergic connections along this tri-synaptic pathway, projections between the two hippocampi are known to exist These are primarily made by GCs, mossy cells (MCs) located in the hilar area (between the CA3c region and the GC layer of the DG) and CA3c-PCs (Swanson et al, 1981; Ribak et al, 1985, 1986). The lateralization of hippocampal function and communication between the two hemispheres, even on a general level, has been examined in very few studies (Czéh et al, 1998; de Hoz et al, 2005; Klur et al, 2009), leaving questions on the nature of commissurally projecting GABAergic cells open
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