Cortical inhibitory neuron basket cells: from circuit function to disruption

Authors

  • Chris J. McBain

    1. Program in Developmental Neurobiology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Porter Neuroscience Building, Rm 3C903, National Institutes of Health, Bethesda, MD 20892, USA
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Email: mcbainc@mail.nih.gov

Despite representing only ∼10–15% of the total cortical and hippocampal neuronal population, local circuit GABAergic inhibitory interneurons represent one of the most diverse cell types in the mammalian central nervous system. In the hippocampal formation alone upwards of 20 distinct cell types have been described, with the number rising each year (Freund & Buzsaki, 1996; Klausberger & Somogyi, 2008; Tricoire et al. 2011). The pressure to diversify is undoubtedly a consequence of the myriad roles played by local circuit interneurons in precisely shaping and modulating features of both local and global circuits. Indeed precision in the circuit largely relies on the laminar positioning of their somato-dendritic axis to receive appropriate afferent input combined with their axonal output, which targets both principal cell and interneuron subcellular compartments.

At the simplest level, perisomatic targeting inhibitory interneurons control cellular and network synchronization and output by dictating and co-ordinating action potential generation (Freund & Buzaki, 1996; Freund & Katona, 2007). These perisomatic targeting or ‘basket cells’ represent one of the most studied interneuron types in recent years, with numerous studies underscoring their important role in the cortical network. Within this class of neurons, two broadly morphologically similar, but neurochemically distinct, cell types exist: the parvalbumin (PV)-containing, fast spiking basket cell and the cholecystokinin (CCK)-containing non-fast spiking basket cells. Despite having similar overlapping afferent input, they appear to exert distinct inhibitory influences over the network as a result of their distinct repertoire of electrophysiological properties, calcium binding proteins, neuropeptide content and receptors for neuromodulators decorating their cell surface.

At the 2011 Society for Neuroscience meeting in Washington, DC The Journal of Physiology gathered together a number of investigators whose interests are focused on the roles played by this particular class of inhibitory interneuron in a symposium entitled Cortical inhibitory neuron basket cells: from circuit function to disruption. The topics covered in this well attended and lively symposium ranged from the embryogenic origins and developmental trajectories of distinct cohorts of basket cells, development of their basic physiological properties, neuromodulation, circuit and network function, and the potential roles they play in disorders of the central nervous system. In this issue of The Journal we are happy to present a number of symposium reports by the speakers highlighting some of these topics.

Marlene Bartos (Bartos & Elgueta, 2012) reports on the synaptic and integrative properties of the two perisomatic inhibitory interneuron types and highlights how their distinct input–output and integrative properties allow them to operate with different speed and precision, thereby allowing them to provide differential contributions to the operations of neuronal networks. Ivan Soltesz (Armstrong & Soltesz, 2012) expands on this topic to discuss how the intrinsic and network properties of each basket cell are sculpted by neuromodulators such as CCK. Specifically, he describes the bidirectional properties of CCK modulation of the two types of basket cell and highlights how not only receptors present on the basket cells themselves shape interneuron function, but how the activity of their downstream targets can manipulate their function by liberating neuromodulators such as endocannabinoids. Ken Pelkey and colleagues (Cea-del Rio et al. 2012) provide a synthesis of both their recent data and associated literature highlighting the differential modulation of these two cell types by the neuromodulator acetylcholine. Tibor Harkany discusses the differential spatial origins of these two interneuron classes and how short range intercellular guidance cues impact the formation and function of GABAergic synapses made by CCK-containing interneurons (Keimpema et al. 2012). Finally, David Lewis (Curley & Lewis, 2012) describes exciting new evidence suggesting that a shift in the relative strengths of PV- versus CCK-containing interneuron transmission may underlie cortical oscillation deficits and working memory impairments in the prefrontal cortex in schizophrenic patients.

Taken together these symposium reviews underscore the recent advances in our understanding of the roles played by these two neuronal populations. As more features of basket cells are illuminated they suggest that not only are their basic physiological properties important for establishing hippocampal and cortical network function, but how neuromodulation of pre- and postsynaptic elements sculpt their roles and collectively how their aberrant development and circuit formation have major roles to play in establishing numerous central nervous system disorders. These are exciting times for inhibitory interneurons that have wisely evolved to not put all of their eggs into one basket.

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