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The Enigmatic Function of Chandelier Cells

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The Enigmatic Function of Chandelier Cells View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central FOCUSED REVIEW published: 08 December 2010 doi: 10.3389/fnins.2010.00201 The enigmatic function of chandelier cells Alan R. Woodruff 1*, Stewart A. Anderson 2 and Rafael Yuste1 1 Department of Biological Sciences, Howard Hughes Medical Institute, Columbia University, New York, NY, USA 2 Department of Psychiatry, Weill Cornell Medical College, Cornell University, New York, NY, USA Chandelier (or axo-axonic) cells are one of the most distinctive GABAergic interneurons in the brain. Their exquisite target specificity for the axon initial segment of pyramidal neurons, together with their GABAergic nature, long suggested the possibility that they provide the ultimate inhibitory control of pyramidal neuron output. Recent findings indicate that their function may be more complicated, and perhaps more interesting, than initially believed. Here we review these recent developments and their implications. We focus in particular on whether chandelier cells may provide a depolarizing, excitatory effect on pyramidal neuron output, in addition to a powerful inhibition. Keywords: GABAergic depolarization, excitation, cortex, axon initial segment INTRODUCTION arborizations of different interneurons reflects The mammalian brain is an organ of seemingly their subcellular target specificity, which in turn impossible complexity. There are billions of neu- has important implications for their function. rons, trillions of synaptic connections, and prob- Indeed, a common delineation exists between ably hundreds of distinct cell types, each of which interneurons targeting dendritic domains, such as is presumably specialized to perform distinct neocortical Martinotti and double bouquet cells, Edited by: tasks. A crucial step in addressing the underly- and those targeting axo-somatic domains, such David Linden, Johns Hopkins University, USA ing logic in the design of the brain is therefore as chandelier and basket cells (Markram et al., identifying the function, or functions, of a given 2004). Whereas dendrite-targeting neurons may Reviewed by: Stephen R. Williams, University of neuronal class. be more suited to modify and gate incoming exci- Cambridge, UK The most obvious separation in neuron func- tatory input (Murayama et al., 2009), axo-somatic Miles A. Whittington, Newcastle tion within cortical structures is between exci- interneurons are likely to exhibit a greater impact University, UK tatory, glutamatergic pyramidal (or principal) on the direct output of the postsynaptic neuron *Correspondence: neurons and inhibitory GABAergic interneurons. (Marr, 1970; Miles et al., 1996). Information is presumably carried and processed Here we focus on attempting to understand by pyramidal (Pyr) neurons, whose connections the chandelier cell (ChCs), an interneuron type traverse cortical layers and regions. Interneurons, that exemplifies the target specificity of cortical by contrast, are typically considered to project interneurons and thus potentially illustrates the only locally, and provide a means of controlling purposeful design of neuronal circuits. ChCs Alan R. Woodruff received his Ph.D. the excitation provided by pyramidal neurons. It were “missed” by Cajal and Lorente and were first from the University of Queensland under is, of course, not that simple. It turns out that a identified by Szentagothai and, independently, by the mentorship of Prof. Pankaj Sah, where he studied the local circuit vast heterogeneity exists amongst the GABAergic Jones (Jones, 1975; Szentagothai, 1975). The defin- properties of GABAergic neurons in the interneurons, which constitute ∼20% of all cor- ing morphological characteristic of ChCs is the basolateral amygdala. His current tical neurons. This heterogeneity has long been array of short, vertically oriented rows of terminal research, at Columbia University with recognized (Ramón y Cajal, 1899; Lorente de Nó, boutons, which resemble candlesticks. Originally Prof. Rafael Yuste, is focused on elucidating the function of cortical 1922), and one of the first aspects of this heteroge- believed to contact the apical dendrite of pyrami- chandelier cells. neity to be noticed, their “short axons,” is likely to dal cells (Szentagothai, 1975), these axonal car- [email protected] be one of the most important – the distinct axonal tridges were later shown via electron microscopic Frontiers in Neuroscience www.frontiersin.org December 2010 | Volume 4 | Article 201 | 1 Woodruff et al. Chandelier cell function Chandelier cell reconstructions of Golgi-stained specimens to nomenclature that is used interchangeably. This GABAergic interneuron whose exclusive exclusively contact the axon initial segment (AIS) highly stereotyped and visually striking appear- postsynaptic target is the axon initial of pyramidal neurons (Figure 1C; Somogyi, 1977; ance of ChCs facilitated early studies regarding segment of pyramidal neurons. Fairen and Valverde, 1980). Because of this, chan- their location, abundance, and neurochemical delier neurons were renamed “axo-axonic cells,” a features. ChCs are present in all cortical layers, AB L1 L2/3 L4 100 µm C D 20 mV 400 pA 100 ms 10 µm ChC BC E F ChC BC -58 mV -59 mV 0.5 mV Record ChC Record BC 50 mV 20 ms ChC 10 ms -66 mV -67 mV BC NBQX -73 mV -72 mV Pyr 5 pA -81 mV -85 mV (rest) (rest) 3.5 ms -91 mV -90 mV FIGURE 1 | Characteristic features of chandelier cells. (A) Neurolucida reconstruction of a layer 2/3 chandelier cell. Cell body and dendrites are in blue, axon in red. Several vertically oriented axonal segments are visible, and are the characteristic morphological feature of ChCs. The long descending axon (arrowhead) reached and arborized in layer 6, but has been digitally truncated. (B) Parvalbumin immunoreactivity of a ChC. A GFP-labeled ChC (right panel, arrow) co-expresses PV (left panel, arrow). (C) Biocytin-filled ChC forms a row of cartridge synapses (arrowheads) on the AIS of a biocytin-filled cortical pyramidal neuron (axon marked by white arrow).(D) Chandelier and basket cells have characteristic responses to threshold current injection. Both cells exhibit the fast-spiking phenotype at higher current intensities (right panel, 2× threshold illustrated). (E) In cortical layer 2/3 pyramids, EGABA differs at ChC–Pyr and BC–Pyr synapses. (F) ChCs can initiate polysynaptic events. Activation of a GABAergic ChC evokes a response in a simultaneously recorded basket cell. The response (left panel) is sensitive to the AMPA receptor antagonist NBQX, has a disynaptic latency, and is observed in a cell type (BC) that receives no direct synapses from ChCs. Schematic of disynaptic circuit is shown in right panel. (B, D and E) modified, fromWoodruff et al. (2009). Frontiers in Neuroscience www.frontiersin.org December 2010 | Volume 4 | Article 201 | 2 Woodruff et al. Chandelier cell function most abundantly in layer 2/3 (DeFelipe et al., and resulted in ChCs being less receptive to 1985; Inda et al., 2007). Although originally ascending sensory input. However, ChCs mark- described in neocortex (Szentagothai, 1975), edly increased their output during conditions of ChCs have also been found in the CA3 (Sik et al., high network activity, implying that ChCs may 1993), CA1 (Somogyi et al., 1983) and dentate be recruited to dampen excessive excitation. gyrus (Soriano and Frotscher, 1989) regions of the Until recently, therefore, all evidence seemed to hippocampus, and in the amygdala (McDonald, suggest that ChCs were inhibitory GABAergic 1982). The expression of GABA (Somogyi et al., neurons, unique in their high degree of spatial 1985), parvalbumin (PV; DeFelipe et al., 1989), target selectivity, but otherwise not particularly and corticotropin-releasing factor (Lewis et al., remarkable in comparison to other GABAergic 1989) provides a neurochemical identity to these cell types. neurons (Figure 1B). Despite this knowledge, it has been signifi- ARE CHANDELIER CELLS DEPOLARIZING? cantly more difficult to ascertain the physiologi- In 2006, a controversial paper appeared demon- cal properties of ChCs, and more particularly strating an excitatory effect of cortical layer 2/3 their putative functions. This is in part due to chandelier cell activation (Szabadics et al., 2006). the rarity of ChCs and the fact that common Three pieces of evidence were presented in sup- markers label both chandelier and the much port of this. Firstly, disynaptic, glutamatergic exci- more abundant basket cells. To date there is cur- tatory postsynaptic potentials (EPSPs) could be rently no known unique ChC marker. Although elicited following a single spike in the chandelier a variety of transgenic mouse lines now exist in cell – an effect attributed to direct recruitment which various populations of interneurons are of pyramidal neurons by ChCs (Figure 1F). But fluorescently labeled, including PV-positive neu- for direct recruitment of a pyramidal neuron to rons (Meyer et al., 2002; Chattopadhyaya et al., occur with such a short latency, the ChC synapse 2004), ChCs have been recorded from much less at the AIS had to be depolarizing, a condition not frequently than have the more numerous basket previously considered for this particular synapse. cells. Physiologically, both ChCs and BCs fire Secondly, the authors confirmed that the ChC high frequency, minimally adapting trains of synapse was indeed depolarizing, with the GABAA narrow action potentials – a fast-spiking pheno- reversal potential (EGABA) significantly elevated type.
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