Firing Patterns Of Interneurons Research Articles

Modulatory Effects of Perineuronal Oligodendrocytes on Neuronal Activity in the Rat Hippocampus.

Action potentials are fundamental to relaying information from region to region in the nervous system. Changes in action potential firing patterns in neural circuits influence how the brain processes information. In our previous study, we focused on interneuron/perineuronal astrocyte pairs in the hippocampal CA1 region and reported that direct depolarization of perineuronal astrocytes modulated the firing pattern of interneurons. In the current study, we investigated the morphological and electrophysiological properties of perineuronal oligodendrocytes, and examined their modulatory effects on interneuronal firing in the CA1 region. Perineuronal oligodendrocytes only had a few processes, which were crooked, intricately twisted, and twined around the soma and proximal region of the main processes of adjacent interneurons. Whole-cell current patterns of perineuronal oligodendrocytes were homogenous and the current-voltage relationship showed remarkable outward rectification. Although the K+ channel blockers, tetraethylammonium and 4-aminopyridine, clearly blocked outward currents, Ba2+ did not significantly alter whole-cell currents. Unlike perineuronal astrocytes, the depolarization of perineuronal oligodendrocytes had no effect on interneuronal firing; however, when the interneurons were firing at a higher frequency, the hyperpolarization of perineuronal oligodendrocytes suppressed their action potentials. The suppressive effects of perineuronal oligodendrocytes were inhibited in the presence of a low concentration of tetraethylammonium, which selectively blocked deep and fast afterhyperpolarization. These results suggest that perineuronal oligodendrocytes suppress interneuronal firing through their influence on K+ channels, which are responsible for deep and fast afterhyperpolarization.

The role of adaptation current in synchronously firing inhibitory neural networks with various topologies

Inhibitory neural networks have the capacity to fire synchronously depending strongly on synaptic current dynamics. Various types of inhibitory interneurons, including some with adaptation currents, are present in hippocampal circuits and are implicated in governing overall network pattern formation. However, the contribution of intrinsic cell firing patterns of interneurons to these patterns has not been fully investigated. Understanding how both synaptic and cellular properties contribute to the propensity for inhibitory neural networks to synchronize is thus an invaluable tool for investigating hippocampal network pattern formation. Through numerical simulation of large, spiking neuron, inhibitory networks, we investigate the role of the slow, adapting M-type K+ current in network pattern formation. This adapting current plays a role in hippocampal interneurons, including the OLM cells, in which the blockade of M-current by acetylcholine or other neurotransmitters switches the neuronal firing rate-current relation (f-I curve) from Type II to Type I. Other types of interneurons, such as fast-spiking PV cells, display Type II f-I curves without any adaptation current. Thus, we consider networks of three cell types: Type I neurons and Type II neurons that either contain [1] or do not contain an M-type K+ adaptation current. All cell types are modeled in the Hodgkin-Huxley formalism. Heterogeneity is introduced to the networks through randomized external applied current to the neurons. We vary network connection topologies using the Small World Network Paradigm [2] in order to systematically investigate the role of connectivity between local and random topologies. To probe the interaction of cellular and synaptic properties influencing synchronization in these networks, we vary the time constant of decay of the inhibitory synaptic current and the intrinsic cellular frequencies by varying the mean of the distribution of external currents applied to each neuron. With sparse, nearest neighbor connection topologies, Type I networks exhibit stationary activity patterns reminiscent of standing waves while Type II neurons exhibit traveling wave activity patterns that sweep across the network. These traveling waves are much more robust and regular when the Type II neurons contain the adaptation current. With sparse random connectivity, Type II networks without an adaptation current exhibit cluster-firing patterns, in which cells segregate into multiple clusters that show synchrony within the cluster but not across clusters. In contrast, Type II networks with the adaptation current display full synchronization for some parameter ranges, but do not exhibit robust clustering (Figure ​(Figure1).1). Preliminary analysis suggests that some of these results are due to the differences between Type I and Type II f-I profiles and that the adaptation current may enhance the effects of these differences. Figure 1 Differential synchronization properties (scored by the Golomb measure [3]) of two inhibitory networks as a function of synaptic current duration, external drive and synaptic strength. In 1000 neuron networks with 300 random incoming synapses per neuron, ...

Dynamic Reconfiguration of Hippocampal Interneuron Circuits during Spatial Learning

SummaryIn the hippocampus, cell assemblies forming mnemonic representations of space are thought to arise as a result of changes in functional connections of pyramidal cells. We have found that CA1 interneuron circuits are also reconfigured during goal-oriented spatial learning through modification of inputs from pyramidal cells. As learning progressed, new pyramidal assemblies expressed in theta cycles alternated with previously established ones, and eventually overtook them. The firing patterns of interneurons developed a relationship to new, learning-related assemblies: some interneurons associated their activity with new pyramidal assemblies while some others dissociated from them. These firing associations were explained by changes in the weight of monosynaptic inputs received by interneurons from new pyramidal assemblies, as these predicted the associational changes. Spatial learning thus engages circuit modifications in the hippocampus that incorporate a redistribution of inhibitory activity that might assist in the segregation of competing pyramidal cell assembly patterns in space and time.

Unilateral lesion of the nigrostriatal pathway decreases the response of interneurons in medial prefrontal cortex to 5-HT 2A/2C receptor stimulation in the rat

The aim of the present study was to investigate changes in the firing rate and pattern of interneurons in the medial prefrontal cortex (mPFC), and effects of 5-HT 2A/2C receptor agonist DOI and antagonist ritanserin, and the selective 5-HT 2C receptor antagonist SB 242084 on the neuronal firing in rats with 6-hydroxydopamine (6-OHDA) lesions of the substantia nigra pars compacta (SNc) by extracellular recording in vivo. The lesion of the SNc decreased the firing rate of the interneurons compared to sham-lesioned rats, and firing pattern of these interneurons changed toward a more burst-firing. Administration of DOI (20–320 μg/kg, i.v.) dose-dependently increased the firing rate of all interneurons examined in sham-lesioned and the 6-OHDA-lesioned rats. The excitation was significant at doses higher than 40 μg/kg and 320 μg/kg in sham-lesioned and the 6-OHDA-lesioned rats, respectively. This dose, which produced marked effect in the 6-OHDA-lesioned rats, was much higher than that of sham-lesioned rats. The local application of DOI (5 μg) in mPFC increased the firing rate of the interneurons in sham-lesioned rats, while having no effect on the firing rate in the 6-OHDA-lesioned rats. The excitatory effect of DOI in sham-lesioned and the 6-OHDA-lesioned rats was completely or partially reversed by ritanserin or SB 242084. The results of our study show that lesion of the SNc leads to a decrease in the firing rate of interneurons in mPFC and fire with a more burst pattern, and decreased response of the interneurons to DOI in rat.

Interplay between subthreshold potentials and γ oscillations in Mauthner cells’ presynaptic inhibitory interneurons

Oscillations are widely distributed throughout the nervous system. A number of models accounting for their generation and their contribution to the synchronization of the concerned neurons, have been proposed. Most of these schemes involve inhibitory interneurons. Here we studied, in vivo, the firing patterns of interneurons, identified as presynaptic to the goldfish Mauthner (M) cell, and called passive hyperpolarizing potential (PHP) cells. We found that a subset of these interneurons was characterized by the presence of subthreshold oscillations of their membrane potential. Such oscillations near the firing threshold generated action potentials that were phased-locked on the oscillations and consequently, the distributions of time intervals between these spikes were observed at integral multiple values of the oscillation cycles. Two superimposed oscillatory processes have been identified. The amplitude of the first one, “the carrier,” was voltage dependent while that of the second, the “modulator,” was not. The frequency of the carrier was distributed among four values (140, 100, 71 or 50 Hz), the frequency of the “modulator” was about 50 Hz in almost all the investigated neurons. The demonstration that the 50 Hz oscillations were shared by almost all PHP exhibiting neurons strongly supports the notion that these cells act synchronously. Finally, auditory stimulations activated “silent” interneurons whereas they inhibited “active” ones, confirming that the presence of oscillations endows the M-cell inhibitory network with dynamic properties which can effectively organize the timing of motor behavior. Our results demonstrate that multiple frequencies, all in the gamma range, can coexist in the same network and that oscillations are present in a well defined population of inhibitory cells that controls fast decision-making.

Membrane properties and synaptic connectivity of fast-spiking interneurons in rat ventral striatum

In vitro patch-clamp recordings were made to study the membrane properties and synaptic connectivity of fast-spiking interneurons in rat ventral striatum. Using a whole-cell configuration in acutely prepared slices , fast-spiking interneurons were recognized based on their firing properties and their morphological phenotype was confirmed by immunocytochemistry. Membrane properties of fast-spiking interneurons were distinguished from those of medium-sized spiny neurons by their more depolarized resting membrane potential, lower action potential amplitude and shorter half-width, short spike repolarization time and deep spike afterhyperpolarization. Firing patterns of interneurons could be subdivided in a bursting and non-bursting mode. Simultaneous dual whole-cell recordings revealed a high degree of connectivity of fast-spiking interneurons to medium-sized spiny neurons via unidirectional synapses. Burst firing in fast-spiking interneurons that were presynaptic to medium-sized spiny neurons resulted in barrages of postsynaptic potentials showing an initial amplitude increment, rapidly followed by a decrement. In conclusion, ventral striatal fast-spiking interneurons can be clearly distinguished from medium-sized spiny neurons by their membrane properties and their firing patterns can be subdivided in bursting and non-bursting modes. Their synaptic connectivity to medium-sized spiny neurons is unidirectional and characterized by frequency-dependent, dynamic changes in postsynaptic amplitude.

Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro.

A variety of population oscillations, at frequencies approximately 5 Hz up to 200 Hz and above, can be induced in hippocampal slices either by (a) manipulation of the ionic environment, or (b) by stimulation of metabotropic receptors; brief oscillations can even occur spontaneously. In this review, we consider in vitro theta (4-12 Hz), gamma/beta (15-70 Hz), and very fast oscillations (VFO) (>70 Hz). Many in vitro oscillations are gated by synaptic inhibition but are influenced by electrical coupling as well; one type depends solely on electrical coupling. For some oscillations dependent upon inhibition, the detailed firing patterns of interneurons can influence long-range synchronization. Two sorts of electrical coupling are important in modulating or generating various in vitro oscillations: (a) between interneurons, primarily between dendrites; and (b) between axons of pyramidal neurons. VFO can exist in isolation or can act as generators of gamma frequency oscillations. Oscillations at gamma frequencies and below probably create conditions under which synaptic plasticity can occur, between selected neurons-even those separated by significant axonal conduction delays.