Distinct Dendritic Arborization andIn VivoFiring Patterns of Parvalbumin-Expressing Basket Cells in the Hippocampal Area CA3

Abstract

Hippocampal CA3 area generates temporally structured network activity such as sharp waves and gamma and theta oscillations. Parvalbumin-expressing basket cells, making GABAergic synapses onto cell bodies and proximal dendrites of pyramidal cells, control pyramidal cell activity and participate in network oscillations in slice preparations, but their roles in vivo remain to be tested. We have recorded the spike timing of parvalbumin-expressing basket cells in areas CA2/3 of anesthetized rats in relation to CA3 putative pyramidal cell firing and activity locally and in area CA1. During theta oscillations, CA2/3 basket cells fired on the same phase as putative pyramidal cells, but, surprisingly, significantly later than downstream CA1 basket cells. This indicates a distinct modulation of CA3 and CA1 pyramidal cells by basket cells, which receive different inputs. We observed unexpectedly large dendritic arborization of CA2/3 basket cells in stratum lacunosum moleculare (33% of length, 29% surface, and 24% synaptic input from a total of ϳ35,000), different from the dendritic arborizations of CA1 basket cells. Area CA2/3 basket cells fired phase locked to both CA2/3 and CA1 gamma oscillations, and increased firing during CA1 sharp waves, thus supporting the role of CA3 networks in the generation of gamma oscillations and sharp waves. However, during ripples associated with sharp waves, firing of CA2/3 basket cells was phase locked only to local but not CA1 ripples, suggesting the independent generation of fast oscillations by basket cells in CA1 and CA2/3. The distinct spike timing of basket cells during oscillations in CA1 and CA2/3 suggests differences in synaptic inputs paralleled by differences in dendritic arborizations.

Fast-spiking, parvalbumin + GABAergic interneurons: From cellular design to microcircuit function

“…PV + interneurons have multiple dendrites which often cross layers (17)(18)(19)(20). This will permit PV + interneurons to receive input from different afferent pathways, such as feedforward and feedback pathways.…”

“…This will permit PV + interneurons to receive input from different afferent pathways, such as feedforward and feedback pathways. The cumulative dendritic length of single PV + interneurons ranges from 3.1 to 9 mm (17)(18)(19)(20). Long dendrites allow PV + interneurons to sample input from a large population of principal cells.…”

“…Finally, somata and dendrites of PV + interneurons are densely covered with synapses. PV + interneurons in the hippocampal CA3 or CA1 region have ~16000-34000 synapses, 94% of which are excitatory and 6% are inhibitory (17,20). A large proportion of inhibitory synapses is PV + (17), but inhibitory inputs from vasoactive intestinal peptide-and somatostatin-expressing interneurons are also present (21,22).…”

Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation

“…Periodic perisomatic inhibition has been held responsible for the generation of the high-frequency components and the phaselocking of neuronal activity [3], but no convincing data are available about the initiation of SWRs, although the SWR state is considered an "off-line" state of the hippocampus [1 2]. To uncover the participation of different types of neurons in SWR generation, several in vivo [28][29][30][31][32][33][34] and in vitro [35][36][37] studies have examined the firing characteristics of identified neuron types (summarized in [38]). Mostly similar relative firing patterns were found for the examined cell types, but there were some contradictory results, which might have arisen from differences between the CA1 and the CA3 area, and most importantly from anaesthetized compared to freely moving animals or in vitro slices.…”

Quantitative ultrastructural analysis of basket and axo-axonic cell terminals in the mouse hippocampus

“…While it is clear that basket cells inhibit their target neurons, the effect of axo-axonic cells is still debated and it can be either excitatory (Szabadics et al, 2006) or inhibitory (Glickfeld et al, 2009). In addition, the three perisomatic interneuron groups are active at different times and show different firing patterns during network oscillations in vivo (Klausberger et al, 2003;Klausberger et al, 2005;Tukker et al, 2007;Lasztóczi et al, 2011;Lapray et al, 2012;Tukker et al, 2013) and also in in vitro preparations Hájos et al, 2013).…”