Stratum oriens horizontal interneurone diversity and hippocampal network dynamics

Abstract

In this last decade, the combination of differential interference contrast infrared video technology and patch-clamp techniques applied to slices in vitro has allowed the routine electrophysiological recording of visually identified central neurones. This has opened the way to the possibility of preselecting GABAergic interneurones of the hippocampus on the basis of some peculiar morphological characteristics. In particular, stratum oriens 'horizontal' interneurones are easily recognizable in living hippocampal slices because of their location and bipolar/bitufted appearance. Thus, this class of cells has rapidly risen as one of the most studied in the entire hippocampus. In this review, I will try to assemble the vast electrophysiological knowledge on these interneurones into a more focused picture, which is relevant for network activity in vitro and in vivo.

Figure 1. Heterogeneity of horizontal stratum oriens interneurones

Despite possessing similar soma and dendrites (red), the specific axonal (black) localization of stratum oriens horizontal neurones defines distinct cell types. Notice, for example, the differences in the reconstructions showing (left to right): an O-LM cell, horizontal (h) basket cell, O-bistratified cell, and a horizontal (h) axo-axonic interneurone. A schematic representation of a CA1 pyramidal neurone is depicted at the left for reference. The borders of the different hippocampal layers are marked by dotted lines. l-m: stratum-lacunosum-moleculare, r: stratum radiatum, p: stratum pyramidale, and o: stratum oriens. Figure from Maccaferri et al. (2000). The horizontal axo-axonic cell was reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc. © 2004 Wiley-Liss, from Ganter et al. (2004).

Figure 2. Pure feedback activation of horizontal cells compared to mixed activation of vertical interneurones

A, after stimulation of stratum radiatum, the EPSP in a horizontal O-LM cell begins after the peak of the population spike recorded in stratum pyramidale, indicating that interneurone activation depends on firing of pyramidal cells. B, in contrast, the EPSP recorded in a stratum oriens basket cell with vertical dendrites begins before the peak of the population spike, indicating feedforward activation. Notice also the notch in the rising phase of the EPSP recorded in the vertical interneurone (arrow), suggesting distinct events mediated by mono- (feedforward) and disynaptic (feedback) inputs. Figure modified and reproduced with permission from Maccaferri & McBain (1996a). © 1996 by the Society for Neuroscience.

Figure 3. Synaptic dynamics of GABAergic unitary connections innervating different postsynaptic domains and activity-dependent shift of recurrent inhibition

A, left, a train of action potentials (top) induced by a current step in a presynaptic horizontal axo-axonic cell induces a transient, depressing summated IPSC in a postsynaptic CA1 pyramidal cell. A single sweep (middle) and the average of many traces (bottom) are shown below. The dotted line indicates the baseline and the peak level of the first event. Right, similarly arranged traces from an O-bistratified → pyramidal neurone unitary connection. A similar train of action potentials (top) induces a non-decremental summated postsynaptic response, as shown by a single sweep (middle) and by the average of many (bottom). Notice that the summated IPSC maintains a level of current similar to the peak of the first response throughout the action potential train. B, activity-dependent shift of postsynaptic inhibition from the perisomatic area to the dendrites. Activation of feedback inhibition by a single shock to the alveus (to activate antidromically the axon of CA1 pyramidal cells) is primarily channelled to the perisomatic area, whereas the last response of a three-shock stimulus at high frequency impacts primarily the dendrites. Traces from a simultaneous somatodendritic recording in a CA1 pyramidal neurone. Panel A is reproduced from Maccaferri et al. (2000). Panel B from Pouille & Scanziani (2004), is reproduced by permission for Nature 429, 717–723, © Macmillan Publishing Ltd (http://www.nature.com).

Figure 4. Cell-type specific synaptic dynamics of horizontal interneurones during synchronized bursting

A, left, simultaneous recording from a CA3 horizontal interneurone (int) and pyramidal cell (pyr) in a hippocampal slice in vitro exposed to elevated external potassium concentrations (8.5 mm). Notice the synchronous bursting and the stronger activity in the interneurone. The right panel shows a burst at a magnified temporal scale: notice that firing in the interneurone precedes firing in the pyramidal cell. B, blocking fast inhibitory synaptic transmission with gabazine reduces the latency to the first spike during a burst in pyramidal cells (pyr), but not interneurones (int). Averaged sweeps of spontaneous bursts recorded in pyramidal cells and interneurones in control (c) and after the addition of gabazine (g). Bursts were artificially aligned on the first spike. Notice that the early phase of the burst leading to the first action potential is subjected to inhibitory control in pyramidal cells, but not interneurones. C, cell-type specific dynamics of GABA_A receptor-mediated inhibition. Voltage-clamp recordings at 0 mV show a different kinetics in pyramidal cells versus interneurones. Notice an early component of the inhibitory waveform that is present in pyramidal cells, but absent in interneurones. Figure modified and reproduced with permission from Aradi & Maccaferri (2004). © 2004 by the Society for Neuroscience.