Basket cell dichotomy in microcircuit function

Abstract

A diversity of GABAergic cell types exist within each brain area, and each cell type is thought to play a unique role in the modulation of principal cell output. Basket cells, whose axon terminals surround principal cell somata and proximal dendrites, have a privileged and influential position for regulating the firing of principal cells. This review explores the dichotomy of the two basket cell classes, cholecystokinin-(CCK) and parvalbumin (PV)-containing basket cells, beginning with differences at the level of the individual cell and subsequently focusing on two ways in which this intrinsic dichotomy is enhanced by extrinsic factors. Neuromodulatory influences, exemplified by the effects of the peptide CCK, dynamically enhance the differential functions of the two cell types. Specifications at the level of the postsynaptic principal cell, including input-specific differences in chloride handling and differences in long-range projection patterns of the principal cell targets, also enhance the distinct network function of basket cells. In this review, new findings will be highlighted concerning the roles of neuromodulatory control and postsynaptic long-range projection pattern in the definition of basket cell function.

Functional Reduction in Cannabinoid-Sensitive Heterotypic Inhibition of Dentate Basket Cells in Epilepsy: Impact on Network Rhythms

“…Additionally, the resulting decrease in FS-BC proximal dendritic input heterogeneity after SE could alter FS-BC excitability (Aradi et al 2004). As in the cortex and hippocampus (Freund 2003;Armstrong and Soltesz 2012), we find cell-specific differences with AC-IN, and not FS-BC, synapses under basal GABA B and CB 1 R regulation of release. Since CB 1 R-expressing neurons receive diverse neuromodulatory inputs (Armstrong and Soltesz 2012), reduction in CB 1 R-sensitive inputs to FS-BCs can isolate FS-BC-based network oscillations from activity or behavioral state-dependent modulation.…”

Dysfunction of hippocampal interneurons in epilepsy

“…For example, the actions of CCK-and PVcontaining basket cells differ in their responses to excitatory input and their functions in neuronal networks, as well as in the pathogenesis of epilepsy, which makes each particularly well-suited to performing different tasks in the regulation of principal cell output [14,15] . PV-expressing basket cells generate trains of short-duration action potentials at high frequencies and provide fast, stable, and timed inhibitory output to their target cells (a highly synchronized GABA release which produce precisely timed inhibition), whereas CCK-expressing basket cells fi re accommodating spike trains at moderate frequencies and generate an asynchronous, fluctuating, and less timed inhibitory output (action potentials with a longer half-duration that progressively broaden during repetitive activation, resulting in a less timed transduction of the signal from the input to the output site) [16] .…”

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

“…In addition, CCK/CB 1 -positive basket cells have two nonoverlapping subgroups: one of them contain vasoactive intestinal polypeptide (VIP) (Acsády et al, 1996), whereas the other subgroup expresses vesicular glutamate transporter 3 (vGluT3) (Somogyi et al, 2004). Several other differences of their molecular composition, intrinsic features, input and output properties have already been described in detail (Glickfeld and Scanziani, 2006;Armstrong and Soltesz, 2012;Bartos and Elgueta, 2012). Briefly, in functional terms, while PV-positive basket cells are ideally suited for generating fast network oscillations, CCK/CB 1 -expressing basket cells rather provide a tonic form of inhibition and act as a "fine-tuning device" in the hippocampus (Freund and Katona, 2007).…”

“…Among these cells, perisomatic interneurons specifically target the cell body and adjacent cell membranes of large populations of local principal cells, whereby they control and synchronize their spike output and, as a consequence, significantly determine hippocampal network activity (Cobb et al, 1995;Miles et al, 1996;Ellender et al, 2010). Perisomatic interneurons can be divided into three nonoverlapping and functionally different populations: two types of basket cells target the somatic and proximal dendritic region of principal cells and interneurons (Freund and Katona, 2007;Armstrong and Soltesz, 2012;Bartos and Elgueta, 2012), while axo-axonic cells innervate the axon initial segment (AIS) of principal cells (Somogyi, 1977).…”