Zachary P. Kilpatrick

Spatially structured oscillations in a two-dimensional excitatory neuronal network with synaptic depression

We study the spatiotemporal dynamics of a two-dimensional excitatory neuronal network with synaptic depression. Coupling between populations of neurons is taken to be nonlocal, while depression is taken to be local and presynaptic. We show that the network supports a wide range of spatially structured oscillations, which are suggestive of phenomena seen in cortical slice experiments and in vivo. The particular form of the oscillations depends on initial conditions and the level of background noise. Given an initial, spatially localized stimulus, activity evolves to a spatially localized oscillating core that periodically emits target waves. Low levels of noise can spontaneously generate several pockets of oscillatory activity that interact via their target patterns. Periodic activity in space can also organize into spiral waves, provided that there is some source of rotational symmetry breaking due to external stimuli or noise. In the high gain limit, no oscillatory behavior exists, but a transient stimulus can lead to a single, outward propagating target wave.

Traveling pulses and wave propagation failure in inhomogeneous neural media

We use averaging and homogenization theory to study the propagation of traveling pulses in an inhomogeneous excitable neural network. The network is modeled in terms of a nonlocal integro- differential equation, in which the integral kernel represents the spatial distribution of synaptic weights. We show how a spatially periodic modulation of homogeneous synaptic connections leads to an effective reduction in the speed of a traveling pulse. In the case of large amplitude modulations, the traveling pulse represents the envelope of a multibump solution, in which individual bumps are nonpropagating and transient. The appearance (disappearance) of bumps at the leading (trailing) edge of the pulse generates the coherent propagation of the pulse. Wave propagation failure occurs when activity is insufficient to maintain bumps at the leading edge.

Binocular Rivalry in a Competitive Neural Network with Synaptic Depression

We study binocular rivalry in a competitive neural network with synaptic depression. In particular, we consider two coupled hypercolums within primary visual cortex (V1), representing orientation selective cells responding to either left or right eye inputs. Coupling between hypercolumns is dominated by inhibition, especially for neurons with dissimilar orientation preferences. Within hypercolumns, recurrent connectivity is excitatory for similar orientations and inhibitory for different orientations. All synaptic connections are modifiable by local synaptic depression. When the hypercolumns are driven by orthogonal oriented stimuli, it is possible to induce oscillations that are representative of binocular rivalry. We first analyze the occurrence of oscillations in a space-clamped version of the model using a fast-slow analysis, taking advantage of the fact that depression evolves much slower than population activity. We then analyze the onset of oscillations in the full spatially extended system by carr...

Sparse gamma rhythms arising through clustering in adapting neuronal networks.

Gamma rhythms (30–100 Hz) are an extensively studied synchronous brain state responsible for a number of sensory, memory, and motor processes. Experimental evidence suggests that fast-spiking interneurons are responsible for carrying the high frequency components of the rhythm, while regular-spiking pyramidal neurons fire sparsely. We propose that a combination of spike frequency adaptation and global inhibition may be responsible for this behavior. Excitatory neurons form several clusters that fire every few cycles of the fast oscillation. This is first shown in a detailed biophysical network model and then analyzed thoroughly in an idealized model. We exploit the fact that the timescale of adaptation is much slower than that of the other variables. Singular perturbation theory is used to derive an approximate periodic solution for a single spiking unit. This is then used to predict the relationship between the number of clusters arising spontaneously in the network as it relates to the adaptation time constant. We compare this to a complementary analysis that employs a weak coupling assumption to predict the first Fourier mode to destabilize from the incoherent state of an associated phase model as the external noise is reduced. Both approaches predict the same scaling of cluster number with respect to the adaptation time constant, which is corroborated in numerical simulations of the full system. Thus, we develop several testable predictions regarding the formation and characteristics of gamma rhythms with sparsely firing excitatory neurons.

Wandering Bumps in Stochastic Neural Fields

We study the effects of noise on stationary pulse solutions (bumps) in spatially extended neural fields. The dynamics of a neural field is described by an integrodifferential equation whose integral term characterizes synaptic interactions between neurons in different spatial locations of the network. Translationally symmetric neural fields support a continuum of stationary bump solutions, which may be centered at any spatial location. Random fluctuations are introduced by modeling the system as a spatially extended Langevin equation whose noise term we take to be multiplicative or additive. For nonzero noise, these bumps are shown to wander about the domain in a purely diffusive way. We can approximate the effective diffusion coefficient using a small noise expansion. Upon breaking the (continuous) translation symmetry of the system using a spatially heterogeneous inputs or synapses, bumps in the stochastic neural field can become temporarily pinned to a finite number of locations in the network. In the case of spatially heterogeneous synaptic weights, as the modulation frequency of this heterogeneity increases, the effective diffusion of bumps in the network approaches that of the network with spatially homogeneous weights.

TWO-DIMENSIONAL BUMPS IN PIECEWISE SMOOTH NEURAL FIELDS WITH SYNAPTIC DEPRESSION ∗

We analyze radially symmetric bumps in a two-dimensional piecewise-smooth neural field model with synaptic depression. The continuum dynamics is described in terms of a nonlocal integrodifferential equation, in which the integral kernel represents the spatial distribution of synaptic weights between populations of neurons whose mean firing rate is taken to be a Heaviside function of local activity. Synaptic depression dynamically reduces the strength of synaptic weights in response to increases in activity. We show that in the case of a Mexican hat weight distribution, sufficiently strong synaptic depression can destabilize a stationary bump solution that would be stable in the absence of depression. Numerically it is found that the resulting instability leads to the formation of a traveling spot. The local stability of a bump is determined by solutions to a system of pseudolinear equations that take into account the sign of perturbations around the circular bump boundary.

Optimizing Working Memory with Heterogeneity of Recurrent Cortical Excitation

A neural correlate of parametric working memory is a stimulus-specific rise in neuron firing rate that persists long after the stimulus is removed. Network models with local excitation and broad inhibition support persistent neural activity, linking network architecture and parametric working memory. Cortical neurons receive noisy input fluctuations that cause persistent activity to diffusively wander about the network, degrading memory over time. We explore how cortical architecture that supports parametric working memory affects the diffusion of persistent neural activity. Studying both a spiking network and a simplified potential well model, we show that spatially heterogeneous excitatory coupling stabilizes a discrete number of persistent states, reducing the diffusion of persistent activity over the network. However, heterogeneous coupling also coarse-grains the stimulus representation space, limiting the storage capacity of parametric working memory. The storage errors due to coarse-graining and diffusion trade off so that information transfer between the initial and recalled stimulus is optimized at a fixed network heterogeneity. For sufficiently long delay times, the optimal number of attractors is less than the number of possible stimuli, suggesting that memory networks can under-represent stimulus space to optimize performance. Our results clearly demonstrate the combined effects of network architecture and stochastic fluctuations on parametric memory storage.

Hallucinogen persisting perception disorder in neuronal networks with adaptation

We study the spatiotemporal dynamics of neuronal networks with spike frequency adaptation. In particular, we compare the effects of adaptation being either a linear or nonlinear function of neural activity. We find that altering parameters controlling the strength of synaptic connections in the network can lead to spatially structured activity suggestive of symptoms of hallucinogen persisting perception disorder (HPPD). First, we study how both networks track spatially homogeneous flickering stimuli, and find input is encoded as continuous at lower flicker frequencies when the network’s synapses exhibit more net excitation. Mainly, we study instabilities of stimulus-driven traveling pulse solutions, representative of visual trailing phenomena common to HPPD patients. Visual trails are reported as discrete afterimages in the wake of a moving input. Thus, we analyze several solutions arising in response to moving inputs in both networks: an ON state, stimulus-locked pulses, and traveling breathers. We find traveling breathers can arise in both networks when an input moves beyond a critical speed. These possible neural substrates of visual trails occur at slower speeds when the modulation of synaptic connectivity is increased.

Stochastic Models of Evidence Accumulation in Changing Environments

Organisms and ecological groups accumulate evidence to make decisions. Classic experiments and theoretical studies have explored this process when the correct choice is fixed during each trial. However, we live in a constantly changing world. What effect does such impermanence have on classical results about decision making? To address this question we use sequential analysis to derive a tractable model of evidence accumulation when the correct option changes in time. Our analysis shows that ideal observers discount prior evidence at a rate determined by the volatility of the environment, and the dynamics of evidence accumulation is governed by the information gained over an average environmental epoch. A plausible neural implementation of an optimal observer in a changing environment shows that, in contrast to previous models, neural populations representing alternate choices are coupled through excitation. Our work builds a bridge between statistical decision making in volatile environments and stochast...

Encoding certainty in bump attractors

Persistent activity in neuronal populations has been shown to represent the spatial position of remembered stimuli. Networks that support bump attractors are often used to model such persistent activity. Such models usually exhibit translational symmetry. Thus activity bumps are neutrally stable, and perturbations in position do not decay away. We extend previous work on bump attractors by constructing model networks capable of encoding the certainty or salience of a stimulus stored in memory. Such networks support bumps that are not only neutrally stable to perturbations in position, but also perturbations in amplitude. Possible bump solutions then lie on a two-dimensional attractor, determined by a continuum of positions and amplitudes. Such an attractor requires precisely balancing the strength of recurrent synaptic connections. The amplitude of activity bumps represents certainty, and is determined by the initial input to the system. Moreover, bumps with larger amplitudes are more robust to noise, and over time provide a more faithful representation of the stored stimulus. In networks with separate excitatory and inhibitory populations, generating bumps with a continuum of possible amplitudes, requires tuning the strength of inhibition to precisely cancel background excitation.