Local circuitry involving parvalbumin‐positive basket cells in the CA2 region of the hippocampus

Abstract

There is a growing recognition that the CA2 region of the hippocampus has its own distinctive properties, inputs, and pathologies. The dendritic and axonal patterns of some interneurons in this region are also strikingly different from those described previously in CA1 and CA3. The local circuitry in this region, however, had yet to be studied in detail. Accordingly, using dual intracellular recordings and biocytin-filling, excitatory and inhibitory connections involving CA2 parvalbumin-positive basket cells were characterized for the first time. CA2 basket cells targeted neighboring pyramidal cells and received excitatory inputs from them. CA2 basket cells that resembled those in CA1 with a fast spiking behavior and dendritic tree confined to the region of origin received depressing excitatory postsynaptic potentials (EPSPs). In contrast, unlike CA1 basket cells but like CA1 Oriens-Lacunosum Moleculare (OLM) cells, the majority of CA2 basket cells had horizontally oriented dendrites in Stratum Oriens (SO), which extended into all three CA subfields, had an adapting firing pattern, presented a "sag" in their voltage responses to hyperpolarizing current injection, and received facilitating EPSPs. The expression of I(h) did not influence the EPSP time courses and paired pulse ratios (PPR). Estimates of the probability of release (p) for the depressing and facilitating EPSPs were correlated with the PPR. Connections with low probabilities of release had higher PPR. Quantal amplitude (q) for the facilitating connections was larger than q at depressing inputs onto fast spiking basket cells.

Updating hippocampal representations: CA2 joins the circuit

“…Further, Schaffer collateral synapses onto CA2 pyramidal neurons do not exhibit experimentally-induced plasticity as readily as those in CA1 or CA3 [55], potentially because of increased spine calcium buffering [56]. CA2 interneurons and their synapses with local pyramidal cells also show unique physiological signatures [57,58], which suggest that CA2 can inhibit CA3 and CA1 in a feedback and feed-forward manner, respectively.…”

“…Reciprocal DG-CA3 loops are certainly likely to be central to iterative processing during pattern separation and completion [4,119], and present another example in which the likelihood and direction of information flow is critically and dynamically dependent upon excitatory-inhibitory tuning. The roles of CA2 in this routing are yet to be explored, but the unique connectivity of its interneuronal populations [57,58] mean its inhibitory influence over CA3 and CA1 must be considered alongside its excitatory projections.…”

Investigation of the hippocampal information processing in freely moving rats

“…The hypothesized population burst-triggering ability of the CA2 circuit might be explained by its unique anatomical wiring ( Figure 1B). In addition to local feedback excitation, CA2 interneurons were also activated by CA1 and CA3 pyramidal neurons, in agreement with anatomical and physiological findings (Bartesaghi et al, 2006;Mercer et al, 2012;Chevaleyre, 2012, 2013). Phasic (superficial) CA2 pyramidal cells were more effective in driving local interneurons compared to their ramping (deep) peers ( Figure 6D), a feature that they share with the CA1 region (Lee et al, 2014;Valero et al, 2015).…”

“…They also receive input from dentate gyrus granule cells, but they lack the thorny excrescences characteristic of the CA3 neurons . In addition to local inputs, CA2 interneurons receive excitation from CA1, CA3, the supramamillary body, and the amygdala (Bartesaghi et al, 2006;Benes and Berretta, 2001;Cui et al, 2013;Ding et al, 2010;Magló czky et al, 1994;Mercer et al, 2012;Chevaleyre, 2012, 2013) and form a loop with layer II entorhinal neurons Rowland and Moser, 2013). In addition to these anatomical differences, recent studies have pointed out the special cognitive and behavioral functions of the CA2 region , including its postulated role in social recognition Piskorowski et al, 2016;Smith et al, 2016), contextual memory Wintzer et al, 2014), and temporal coding .…”

Synaptic integration by different dendritic compartments of hippocampal CA1 and CA2 pyramidal neurons

“…This high density of interneurons in the CA2 region might also apply in rodents, at least for interneurons expressing somatostatin (see reference [80]). In addition, the probability of obtaining a whole-cell recording between a connected interneuron and pyramidal cell is higher in CA2 than in CA1 [81], suggesting a stronger inhibitory drive. Finally, a unique type of interneuron with wide dendritic and axonal projections has been reported in CA2 [81].…”