Functional characteristics of parvalbumin- and cholecystokinin-expressing basket cells - PubMed (original) (raw)
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Functional characteristics of parvalbumin- and cholecystokinin-expressing basket cells
Marlene Bartos et al. J Physiol. 2012.
Abstract
Cortical neuronal network operations depend critically on the recruitment of GABAergic interneurons and the properties of their inhibitory output signals. Recent evidence indicates a marked difference in the signalling properties of two major types of perisomatic inhibitory interneurons, the parvalbumin- and the cholecystokinin-containing basket cells. Parvalbumin-expressing basket cells are rapidly recruited by excitatory synaptic inputs, generate high-frequency trains of action potentials, discharge single action potentials phase-locked to fast network oscillations and provide fast, stable and timed inhibitory output onto their target cells. In contrast, cholecystokinin-containing basket cells are recruited in a less reliable manner, discharge at moderate frequencies with single action potentials weakly coupled to the phases of fast network oscillations and generate an asynchronous, fluctuating and less timed inhibitory output. These signalling modes are based on cell type-dependent differences in the functional and plastic properties of excitatory input synapses, integrative qualities and in the kinetics and dynamics of inhibitory output synapses. Thus, the two perisomatic inhibitory interneuron types operate with different speed and precision and may therefore contribute differently to the operations of neuronal networks.
Figures
Figure 1. Morphological and physiological characteristics of parvalbumin- and cholecystokinin-expressing basket cells
A, top, parvalbumin expressing (PV)-BCs show a high frequency and non-accommodating discharge pattern and selectively express the calcium binding protein paravalbumin (PV) (right). Bottom, reconstruction of an intracellularly labeled PV-BC in CA1 with axon collaterals mostly restricted to the pyramidal cell layer (Str. Pyr.) B, top, cholecystokinin expressing (CCK)-BCs show a slow and accommodating train of action potentials when depolarized by suprathreshold current injection and express high levels of the neuropeptide cholecystokinin (CCK) as revealed by antibody labelling (right). Bottom, reconstruction of an intracellularly labeled CCK-BC shows that there are no apparent morphological differences to PV-BCs. C, left, representative paired recording of a presynaptic CCK-BC and the postsynaptic principal cell. Single action potentials (top) evoke unitary IPSCs (bottom). CCK-BCs can be identified by their sensitivity to depolarization induced suppression of inhibition (DSI; green; control IPSC, black; recovered IPSC, grey). Right, same experimental configuration as left with a presynaptic PV-BC. Note, the lack of DSI at PV-BC output synapses. Bottom, schematic illustration of the molecular mechanisms underlying DSI. Strong activation of pyramidal cells evokes the release of endogenous cannabinoids that retrogradely activate G-protein coupled cannabinoid receptors (CB1Rs) at CCK-BC terminals, thereby inhibiting GABA release. A and B reproduced from Lee et al. (2011) with permission from the Society for Neuroscience; C reproduced from Glickfeld & Scanziani, (2006) with permission from Macmillan Publishers Ltd, _Nature Neuroscience_©2006.
Figure 2. Synaptic excitation, integration and recruitment of basket cells
A, top left, schematic illustration of the major excitatory pathways converging onto PV- (blue) and CCK-BCs (red) in CA1. Middle left, extracellular stimulation of Schaffer collaterals induce EPSCs with amplitudes several times larger in CB1R-negative expressing (CB1R−) PV-BCs than in CB1R-positive expressing (CB1R+) CCK-BCs. EPSCs recorded in BCs were normalized to simultaneously recorded EPSCs in pyramidal cells (Pyr). Bottom left, plot summarizing the relationship between EPSCs recorded in both BC types and in pyramidal cells upon perforant path (PP) or Schaffer collateral (SC) stimulation. Top right, stimulation of the alveus at 20 Hz induces EPSCs with markedly stronger multiple-pulse depression in postsynaptic CCK-BCs (red traces) than in PV-BCs (blue traces). Bottom right, suprathreshold alveus stimulation at 20 Hz only transiently recruits CCK-BCs but allows continuous action potential generation in PV-BCs. B, top left, schematic illustration of the experimental design. Top right, integration of synaptic inputs was tested by SC stimulation at t = 0 ms (black arrow) paired with alveus stimulation at step-wise increasing time delays in relation to SC activation. Bottom, summary plot showing that CCK-BCs summate both inputs over longer inter-stimulus intervals than PV-BCs. Reproduced from Glickfeld & Scanziani (2006) with permission from Macmillan Publishers Ltd, _Nature Neuroscience_©2006.
Figure 5. Differential contribution of PV-BCs and CCK-BCs in the emergence of network oscillations
A, left, cell attached recordings from identified CA3 PV- and CCK-BCs and local field potential recordings during in vitro carbachol-evoked gamma oscillations in hippocampal slices. Middle, bar graphs summarizing the number of action potentials per gamma cycle and their phase-coupling strength of both BC types. Right, bath-application of DAMGO, a μ-opioid agonist that selectively inhibits GABA release at PV-BC output synapses, abolishes carbachol-induced gamma oscillations. B, left, top, diagram of the experimental design: in vivo extracellular recording of gamma oscillations in the prefrontal cortex of mice during activation of channelrhodopsin (ChR2)-expressing pyramidal cell (PY) with blue light and simultaneous activation of halorhodopsin (eNpHR)-containing PV-BCs with yellow light. Left, bottom, activation of eNpHR reduces action potential generation in PV-BCs. Right, top, filtered local field potential recordings in absence (red) or presence (black) of PV-cell activity. Right, bottom, summary plot of the PV-BC effect on gamma power. C, schematic diagram illustrating the hypothetical contribution of CCK-BCs on sparse coding in CA1 principal cells (PC). Timing of action potentials generated in PCs, CCK-BCs and PV-BCs is shown in relation to the phase of fast hippocampal network oscillations. A reproduced from Gulyás et al. (2010) with permission from the Society for Neuroscience; B reproduced from Sohal et al. (2009) with permission from Macmillan Publishers Ltd, _Nature_©2009; and C reproduced from Klausberger et al. (2005) with permission from the Society for Neuroscience.
Figure 3. Distinct AMPA receptor subunit compositions determine different plastic properties in PV-BCs and CCK-BCs
A, top left, intracellular labelling of a PV-BC in rat dentate gyrus (DG). Top right, extracellular stimulation of mossy fibres (MFs) activates AMPAR-mediated EPSCs with inwardly rectifying current–voltage (I–V) relationships. EPSCs mediated by Ca2+ permeable (CP)-AMPARs as indicated by their sensitivity to philantotoxin (PhTx). Bottom, associative high frequency stimulation of MFs induces long term potentiation at PV-BC (red) input synapses, but the same protocol applied to the perforant path is unable to do so (blue). B, top left, reconstruction of a CA1 CCK-BC. Top right, extracellular stimulation at the alveus induces EPSCs in CCK-BCs with linear I–V relation (red line and traces). EPSCs are mediated by Ca2+ impermeable (CI)-AMPARs as further indicated by the lack of PhTx sensitivity. Bottom, CA1 PV-BCs express long term potentiation after applying a non-associative high frequency stimulation to recurrent pyramidal cell (PC) inputs. In contrast, the same stimulation does not induce plastic changes at PC to CCK-BC synapses. Scale bars 100 μm. A reproduced from Sambandan et al. (2010) and B from Nissen et al. (2010) with permission from the Society for Neuroscience.
Figure 4. PV- and CCK-BCs differ in basic properties of GABA release
A, top, paired recordings from a presynaptic PV-BC and a postsynaptic granule cell (GC; left) and a CCK-interneuron to GC pair (right) in the DG. Note differences in the timing of IPSCs and fluctuations in the amplitude. Bottom, 50 Hz trains of action potentials in presynaptic BCs induce fast and synchronized IPSCs at PV-BC to GC synapses but asynchronous IPSCs at CCK-interneuron output synapses. B, top, bar graph summarizing the ratio of synchronous to asynchronous GABA release ratio (synch./asynch. release) evoked by trains of 25 action potentials at 50 Hz for different presynaptic interneuron types (BSC, bistratified cell; TLC, trilaminar cell). Note, asynchronous release depends on the nature of the presynaptic interneuron but is independent of the identity of the target cell. Bottom, naturally occurring spike trains (5 bursts of 5 spikes at 50 Hz) in CCK expressing interneurons generate a continuous barrage of IPSCs in postsynaptic pyramidal cells (PCs). A reproduced from Hefft & Jonas (2005) with permission from Macmillan Publishers Ltd, _Nature Neuroscience_©2005; B reproduced from Daw et al. (2009) with permission from the Society for Neuroscience.
References
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