Loss of synchrony in an inhibitory network of type-I oscillators

Synchronization of excitable cells coupled by reciprocal inhibition is a topic of significant interest due to the important role that inhibitory synaptic interaction plays in the generation and regulation of coherent rhythmic activity in a variety of neural systems. While recent work revealed the synchronizing influence of inhibitory coupling on the dynamics of many networks, it is known that strong coupling can destabilize phase-locked firing. Here we examine the loss of synchrony caused by an increase in inhibitory coupling in networks of type-I Morris-Lecar model oscillators, which is characterized by a period-doubling cascade and leads to mode-locked states with alternation in the firing order of the two cells, as reported recently by Maran and Canavier (2007) for a network of Wang-Buzsáki model neurons. Although alternating- order firing has been previously reported as a near-synchronous state, we show that the stable phase difference between the spikes of the two Morris-Lecar cells can constitute as much as 70% of the unperturbed oscillation period. Further, we examine the generality of this phenomenon for a class of type-I oscillators that are close to their excitation thresholds, and provide an intuitive geometric description of such leap-frog dynamics. In the Morris-Lecar model network, the alternation in the firing order arises under the condition of fast closing of K+ channels at hyperpolarized potentials, which leads to slow dynamics of membrane potential upon synaptic inhibition, allowing the presynaptic cell to advance past the postsynaptic cell in each cycle of the oscillation. Further, we show that non-zero synaptic decay time is crucial for the existence of leap-frog firing in networks of phase oscillators. However, we demonstrate that leap-frog spiking can also be obtained in pulse-coupled inhibitory networks of one-dimensional oscillators with a multi-branched phase domain, for instance in a network of quadratic integrate-and-fire model cells. Also, we show that the entire bifurcation structure of the network can be explained by a simple scaling of the STRC (spike- time response curve) amplitude, using a simplified quadratic STRC as an example, and derive the general conditions on the shape of the STRC function that leads to leap-frog firing. Further, for the case of a homogeneous network, we establish quantitative conditions on the phase resetting properties of each cell necessary for stable alternating-order spiking, complementing the analysis of Goel and Ermentrout (2002) of the order-preserving phase transition map. We show that the extension of STRC to negative values of phase is necessary to predict the response of a model cell to several close non-weak perturbations. This allows us for instance to accurately describe the dynamics of non-weakly coupled network of three model cells. Finally, the phase return map is also extended to the heterogenous network, and is used to analyze both the order-alternating firing and the order-preserving non-zero phase locked state in this case

Shared inputs, entrainment, and desynchrony in elliptic bursters: from slow passage to discontinuous circle maps

What input signals will lead to synchrony vs. desynchrony in a group of biological oscillators? This question connects with both classical dynamical systems analyses of entrainment and phase locking and with emerging studies of stimulation patterns for controlling neural network activity. Here, we focus on the response of a population of uncoupled, elliptically bursting neurons to a common pulsatile input. We extend a phase reduction from the literature to capture inputs of varied strength, leading to a circle map with discontinuities of various orders. In a combined analytical and numerical approach, we apply our results to both a normal form model for elliptic bursting and to a biophysically-based neuron model from the basal ganglia. We find that, depending on the period and amplitude of inputs, the response can either appear chaotic (with provably positive Lyaponov exponent for the associated circle maps), or periodic with a broad range of phase-locked periods. Throughout, we discuss the critical underlying mechanisms, including slow-passage effects through Hopf bifurcation, the role and origin of discontinuities, and the impact of noiseComment: 17 figures, 40 page

On the interaction of gamma-rhythmic neuronal populations

Local gamma-band (~30-100Hz) oscillations in the brain, produced by feedback inhibition on a characteristic timescale, appear in multiple areas of the brain and are associated with a wide range of cognitive functions. Some regions producing gamma also receive gamma-rhythmic input, and the interaction and coordination of these rhythms has been hypothesized to serve various functional roles. This thesis consists of three stand-alone chapters, each of which considers the response of a gamma-rhythmic neuronal circuit to input in an analytical framework. In the first, we demonstrate that several related models of a gamma-generating circuit under periodic forcing are asymptotically drawn onto an attracting invariant torus due to the convergence of inhibition trajectories at spikes and the convergence of voltage trajectories during sustained inhibition, and therefore display a restricted range of dynamics. In the second, we show that a model of a gamma-generating circuit under forcing by square pulses cannot maintain multiple stably phase-locked solutions. In the third, we show that a separation of time scales of membrane potential dynamics and synaptic decay causes the gamma model to phase align its spiking such that periodic forcing pulses arrive under minimal inhibition. When two of these models are mutually coupled, the same effect causes excitatory pulses from the faster oscillator to arrive at the slower under minimal inhibition, while pulses from the slower to the faster arrive under maximal inhibition. We also show that such a time scale separation allows the model to respond sensitively to input pulse coherence to an extent that is not possible for a simple one-dimensional oscillator. We draw on a wide range of mathematical tools and structures including return maps, saltation matrices, contraction methods, phase response formalism, and singular perturbation theory in order to show that the neuronal mechanism of gamma oscillations is uniquely suited to reliably phase lock across brain regions and facilitate the selective transmission of information

Deterministic and stochastic dynamics of multi-variable neuron models : resonance, filtered fluctuations and sodium-current inactivation

Neurons are the basic elements of the networks that constitute the computational units of the brain. They dynamically transform input information into sequences of electrical pulses. To conceive the complex function of the brain, it is crucial to understand this transformation and identify simple neuron models which accurately reproduce the known features of biological neurons. This thesis addresses three different features of neurons. We start by exploring the effect of subthreshold resonance on the response of a periodically forced neuron using a simple threshold model. The response is studied in terms of an implicit one-dimensional time map that corresponds to the Poincar´e map of the forced system. Qualitatively distinct responses are found, including mode locking and chaos. We analytically find the stability regions of mode-locking solutions, and identify the transition to chaos through period-adding bifurcations. We show that the response becomes chaotic when the forcing frequency is close to the resonant frequency. Then we will consider an experimentally verified model with realistic spikegenerating mechanism and study the effect of filtered synaptic fluctuations on the firing-rate response of the neuron. Using a population density method as well as an efficient numerical method, we find the steady-state firing rate in two limits of fast and slow synaptic inputs and present the linear response theory for the firing rate of the model in response to both time-dependent mean inputs and time-dependent noise intensity. Finally, a novel model is introduced that incorporates threshold variability of neurons. We determine the modulation of the input-output properties of the model due to oscillatory inputs and in the presence of filtered synaptic fluctuations.EThOS - Electronic Theses Online ServiceUniversity of WarwickOverseas Research Students Awards Scheme (ORSAS)GBUnited Kingdo

Stability Analysis of Phase-Locked Bursting in Inhibitory Neuron Networks

Networks of neurons, which form central pattern generators (CPGs), are important for controlling animal behaviors. Of special interest are configurations or CPG motifs composed of reciprocally inhibited neurons, such as half-center oscillators (HCOs). Bursting rhythms of HCOs are shown to include stable synchrony or in-phase bursting. This in-phase bursting can co-exist with anti-phase bursting, commonly expected as the single stable state in HCOs that are connected with fast non-delayed synapses. The finding contrasts with the classical view that reciprocal inhibition has to be slow or time-delayed to synchronize such bursting neurons. Phase-locked rhythms are analyzed via Lyapunov exponents estimated with variational equations, and through the convergence rates estimated with Poincar\\u27e return maps. A new mechanism underlying multistability is proposed that is based on the spike interactions, which confer a dual property on the fast non-delayed reciprocal inhibition; this reveals the role of spikes in generating multiple co-existing phase-locked rhythms. In particular, it demonstrates that the number and temporal characteristics of spikes determine the number and stability of the multiple phase-locked states in weakly coupled HCOs. The generality of the multistability phenomenon is demonstrated by analyzing diverse models of bursting networks with various inhibitory synapses; the individual cell models include the reduced leech heart interneuron, the Sherman model for pancreatic beta cells, the Purkinje neuron model and Fitzhugh-Rinzel phenomenological model. Finally, hypothetical and experiment-based CPGs composed of HCOs are investigated. This study is relevant for various applications that use CPGs such as robotics, prosthetics, and artificial intelligence