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Jochen F Staiger

Publications and source records attributed to Jochen F Staiger.

9 recordsLinked to original sources

Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells.

Previous analyses of the spiny layer IV neurons have almost exclusively focused on spiny stellate cells. Here we provide detailed morphological data characterizing three subpopulations of spiny neurons in slices of adolescent rats: (i) spiny stellate cells (58%), (ii) star pyramidal cells (25%) and (iii) pyramidal cells (17%), which can be distinguished objectively by the preferential orientation of their dendritic stems. Spiny stellate cells lacked an apical dendrite and frequently confined their dendritic and axonal arbors to the respective column. Star pyramidal and pyramidal cells possessed an apical dendrite, which reached the supragranular layers. Their axonal arbors were similar, showing both a columnar component and transcolumnar branches with direct transbarrel projections. However, a small fraction of star pyramidal cells possessed few or even no transcolumnar branches. Electrophysiologically, all three types of neurons were either regular-spiking or intrinsically burst-spiking without a significant relation to the morphological subtypes. The basic synaptic properties of thalamic inputs were also independent of the type of target layer IV spiny neuron. All remained subthreshold and showed paired-pulse depression. In conclusion, the columnar axonal arborization of spiny stellate cells is supplemented by a significant oblique to horizontal projection pattern in pyramidal-like neurons. This offers a structural basis for either segregation or early context-dependent integration of tactile information, in a cell-type specific manner.

Action Potentials↗

Calbindin-containing interneurons are a target for VIP-immunoreactive synapses in rat primary somatosensory cortex.

Inhibitory interneurons in cerebral cortex are morphologically and physiologically extremely heterogeneous. This greatly interferes with an understanding of their functions. Progress has been made by classifying these neurons with the aid of molecular markers, e.g., neuropeptides or calcium-binding proteins, which are reliably expressed by certain subpopulations. We have used this approach to demonstrate an output of a subpopulation of cortical interneurons which express vasoactive intestinal polypeptide (VIP). By double immunostaining and correlated light and electron microscopy, we show that calbindin (CB)-containing interneurons located in layers II-VI of rat barrel cortex are targets of symmetric VIP-immunoreactive synapses. All CB-immunoreactive interneurons showed numerous contacts of VIP boutons on proximal and distal dendritic segments. A great majority of CB-immunoreactive interneurons (214/222) displayed such close appositions with VIP boutons on their soma as well. Quantification revealed that the number of VIP-immunoreactive boutons on CB-immunoreactive somata and dendrites of specified order is comparable for the different cortical layers. In conclusion, all calbindin-containing cortical interneurons seem to be under direct influence of other GABAergic interneurons expressing the peptide VIP. An indirect functional consequence of this may be disinhibition of pyramidal cells, which are considered the major target of calbindin interneurons. However, since the examined types of interneurons are intricately embedded in networks of yet different interneurons, the outcome of these multiple inhibitory interactions is likely to be less simplistic. It may be related to the timing of pyramidal cell discharge within and across layers of cortical columns.

Animals↗

Cell type-specific circuits of cortical layer IV spiny neurons.

Sensory signal processing in cortical layer IV involves two major morphological classes of excitatory neurons: spiny stellate and pyramidal cells. It is essentially unknown how these two cell types are integrated into intracortical networks and whether they play different roles in cortical signal processing. We mapped their cell-specific intracortical afferents in rat somatosensory cortex through a combination of whole-cell patch-clamp recordings and caged glutamate photolysis. Spiny stellate cells received monosynaptic excitation and inhibition originating almost exclusively from neurons located within the same barrel. Pyramidal cells, by contrast, displayed additional excitatory inputs from nongranular layers and from neighboring barrels. Their inhibitory inputs originated, as for spiny stellate cells, mainly from neurons located in the same barrel. These results indicate that spiny stellate cells act predominantly as local signal processors within a single barrel, whereas pyramidal cells globally integrate horizontal and top-down information within a functional column and between neighboring barrels.

Afferent Pathways↗

Distinct local circuits between neocortical pyramidal cells and fast-spiking interneurons in young adult rats.

Connections between layer V pyramidal cells and GABAergic fast-spiking interneurons (pyramidal-FS) were studied by paired recordings combined with morphological analyses in acute neocortical slices from 28- to 52-day-old rats. Pairs of spikes elicited in pyramidal cells at a stimulation rate of 0.2 Hz induced unitary excitatory postsynaptic currents (EPSCs) in FS interneurons that displayed facilitation (48%), depression (38.5%), or neither depression nor facilitation (13.5%). Analyses of the EPSC amplitude distributions indicate that depressing connections always showed multiple functional release sites. On the contrary, facilitating connections consisted either of one or several release sites. At a holding potential of -72 mV, the quantal size (q) and the release probability (p) of facilitating connections with a single release site were -21.9 +/- 7.5 pA and 0.49 +/- 0.19 (SD), respectively. The mean q and the estimated number of release sites (n) at connections showing multiple sites were obtained by decreasing the release probability and did not differ between depressing and facilitating synapses (depressing connections: q = -15.3 +/- 2.5 pA, n = 5.1 +/- 3, facilitating connections: q = -23.9 +/- 9.8 pA, n = 7.8 +/- 5.4). However, the quantal content at facilitating synapses with multiple sites (1.9 +/- 1.5) was significantly different from that at depressing connections (4.1 +/- 3.9). Finally, quantitative morphological analyses revealed that most of the pyramidal cells displaying facilitation can be differentiated from those displaying depression by a more densely branched apical dendritic tree. Therefore two types of morphologically distinct pyramidal cells form excitatory connections with FS interneurons that differ in their short-term plasticity characteristics. Facilitating and depressing connections may provide a differential control of the temporal information processing of FS cells and thus finely regulate the inhibitory effect of these interneurons in neocortical networks of young adult rats.

Action Potentials↗

Expression of c-Fos, ICER, Krox-24 and JunB in the whisker-to-barrel pathway of rats: time course of induction upon whisker stimulation by tactile exploration of an enriched environment.

Modified tactile information has been shown to induce adaptive plasticity in the somatosensory cortex of rat. The cellular mechanisms resulting in plastic neuronal responses, however, are largely unknown. Inducible transcription factors have been proposed as one major link in the cascade from modified input to altered neuronal structure and function. We investigated the spatial and temporal patterns of transcription factor induction in the rat whisker-to-barrel pathway by placing the animals in a novel, enriched environment while having clipped sets of whiskers on one side of the face. Such stimulation resulted not only in a specific c-Fos induction in brainstem barrelettes and thalamic barreloids, but also in the barrel-related cortical columns, each with different time courses. In the barrel cortex, c-Fos and Krox-24 immunostaining showed a rapid induction with peak levels at 1 h and a return to basal levels after 14 h. JunB was induced after 1 h of exploration, declined at 6 h and returned to basal levels after this time point. The inducible cyclic AMP early repressor (ICER), a transcription factor of the cAMP signaling pathway, showed a maximum after 6 h, decreased slowly, but elevated levels were still detectable after 5 days. Our data demonstrate that upon whisker stimulation by exploration of a novel, enriched environment, (i) subcortical relay stations in the whisker-to-barrel pathway are able to express elevated levels of c-Fos and (ii) in the barrel cortex c-Fos, JunB, Krox-24 and ICER are differentially regulated in the temporal domain.

Animals↗

Innervation of interneurons immunoreactive for VIP by intrinsically bursting pyramidal cells and fast-spiking interneurons in infragranular layers of juvenile rat neocortex.

Cortical columns contain specific neuronal populations with characteristic sets of connections. This wiring forms the structural basis of dynamic information processing. However, at the single-cell level little is known about specific connectivity patterns. We performed experiments in infragranular layers (V and VI) of rat somatosensory cortex, to clarify further the input patterns of inhibitory interneurons immunoreactive (ir) for vasoactive intestinal polypeptide (VIP). Neurons in acute slices were electrophysiologically characterized using whole-cell recordings and filled with biocytin. This allowed us to determine their firing pattern as regular-spiking, intrinsically bursting and fast-spiking, respectively. Biocytin was revealed histochemically and VIP immunohistochemically. Sections were examined for contacts between the axons of the filled neurons and the VIP-ir targets. Twenty pyramidal cells and five nonpyramidal (inter)neurons were recovered and sufficiently stained for further analysis. Regular-spiking pyramidal cells displayed no axonal boutons in contact with VIP-ir targets. In contrast, intrinsically bursting layer V pyramidal cells showed four putative single contacts with a proximal dendrite of VIP neurons. Fast-spiking interneurons formed contacts with two to six VIP neurons, preferentially at their somata. Single as well as multiple contacts on individual target cells were found. Electron microscopic examinations showed that light-microscopically determined contacts represent sites of synaptic interactions. Our results suggest that, within infragranular local cortical circuits, (i) fast-spiking interneurons are more likely to influence VIP cells than are pyramidal cells and (ii) pyramidal cell input probably needs to be highly convergent to fire VIP target cells.

Action Potentials↗

Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons.

Nicotinic acetylcholine receptors are widely expressed in the neocortex but their functional roles remain largely unknown. Here we investigated the effect of nicotinic receptor activation on interneurons of layer I, which contains a high density of cholinergic fiber terminals. Ninety-seven of 101 neurons recorded in whole cell configuration in rat acute slices were excited by local pressure application of nicotinic agonists, acetylcholine (500 microM), 1,1-dimethyl-4-phenyl-piperazinium (500 microM) or choline (10 mM). Biocytin labeling confirmed that our sample included different morphological types of layer I interneurons. The responses to nicotinic agonists persisted in presence of glutamate and muscarinic receptor antagonists and on further addition of Cd(2+) or tetrodotoxin, indicating that they were mediated by direct activation of postsynaptic nicotinic receptors. The kinetics of the currents and their sensitivity to nicotinic receptor antagonists, methyllycaconitine (1-10 nM) or dihydro-beta-erythroidine (500 nM), suggested that early and late components of the responses were mediated by alpha7 and non-alpha7 types of receptors. Both components had inwardly rectifying I-V curves, which differed when intracellular spermine was omitted. Single-cell RT-PCR experiments identified alpha4, alpha7, and beta2 as the predominantly expressed mRNAs, suggesting that the receptors consisted of alpha7 homomers and alpha4beta2 heteromers. Finally, selective excitation of layer I interneurons through activation of their nicotinic receptors resulted in a tetrodotoxin-sensitive increase of inhibitory synaptic currents recorded in nonpyramidal cells but not in pyramidal cells of layer II/III. These results suggest that acetylcholine released in layer I may induce a disinhibition of the cortical network through activation of nicotinic receptors expressed by layer I interneurons.

Animals↗

Immediate-early gene expression in the barrel cortex.

Since their detection in the early 1980s immediate-early genes (most of them being inducible transcription factors) have been regarded as molecular keys to the orchestration of late-effector genes that ultimately would enable functional and structural adaptation of the brain to changing external and internal demands. This is called neuronal plasticity and it has been intensively studied in the somatosensory (barrel) cortex of rodents. This brain region is intimately involved in the processing and probably also the storage of tactile information, stemming from the large facial whiskers, necessary for object detection or spatial navigation in the environment. On the other hand, several of the inducible transcription factors have been found to function as neuronal activity markers providing a cellular resolution, thus, enabling the cell-type specific mapping of activated neuronal circuits. Some recent data on both topics in the rodent barrel cortex will be presented in this topical review.

Animals↗

Optical release of caged glutamate for stimulation of neurons in the in vitro slice preparation.

Optical stimulation techniques prove useful to map functional inputs in the in vitro brain slice preparation: Glutamate released by a focused beam of UV light induces action potentials, which can be detected in postsynaptic neurons. The direct activation effect is influenced by factors such as compound concentration, focus depth, light absorption in the tissue, and sensitivity of different neuronal domains. We analyze information derived from direct stimulation experiments in slices from rat barrel cortex and construct a computational model of a layer V pyramidal neuron that reproduces the experimental findings. The model predictions concerning the influence of focus depth on input maps and action potential generation are investigated further in subsequent experiments where the focus depth of a high-numerical-aperture lens is systematically varied. With our setup flashes from a xenon light source can activate neuronal compartments to a depth of 200 mum below the surface of the slice. The response amplitude is influenced both by tissue depth and focus plane. Specific somatodendritic structures can be targeted as the probability of action potential induction falls off exponentially with distance. Somata and primary apical dendrites are most sensitive to uncaged glutamate with locally increased sensitivity on proximal apical dendrites. We conclude that optical stimulation can be targeted with high precision.

Action Potentials↗