Pulin Gong

Distributed dynamical computation in neural circuits with propagating coherent activity patterns.

Activity in neural circuits is spatiotemporally organized. Its spatial organization consists of multiple, localized coherent patterns, or patchy clusters. These patterns propagate across the circuits over time. This type of collective behavior has ubiquitously been observed, both in spontaneous activity and evoked responses; its function, however, has remained unclear. We construct a spatially extended, spiking neural circuit that generates emergent spatiotemporal activity patterns, thereby capturing some of the complexities of the patterns observed empirically. We elucidate what kind of fundamental function these patterns can serve by showing how they process information. As self-sustained objects, localized coherent patterns can signal information by propagating across the neural circuit. Computational operations occur when these emergent patterns interact, or collide with each other. The ongoing behaviors of these patterns naturally embody both distributed, parallel computation and cascaded logical operations. Such distributed computations enable the system to work in an inherently flexible and efficient way. Our work leads us to propose that propagating coherent activity patterns are the underlying primitives with which neural circuits carry out distributed dynamical computation.

Emergence of scale-free network with chaotic units

To study the evolution of complex network with dynamical units, in this paper we consider the development of the network with chaotic units. By the addition of new nodes continuously and the adaptive rewiring of the connections according to the dynamic coherence of the activity patterns in the network, we can obtain that the growing network self-organizes into a complex network of which the connectivity distribution reveals a power law, at the same time, the network has a high clustering coefficient and small average shortest path length. The importance of chaos in the emergence of this type of scale-free network is investigated through comparing it to systems of periodic and stochastic units. The functional advantage of the self-organized network with dynamical units is revealed by showing the robustness of the spatiotemporal dynamics of the complex network.

A computational role for bistability and traveling waves in motor cortex

Adaptive changes in behavior require rapid changes in brain states yet the brain must also remain stable. We investigated two neural mechanisms for evoking rapid transitions between spatiotemporal synchronization patterns of beta oscillations (13–30 Hz) in motor cortex. Cortex was modeled as a sheet of neural oscillators that were spatially coupled using a center-surround connection topology. Manipulating the inhibitory surround was found to evoke reliable transitions between synchronous oscillation patterns and traveling waves. These transitions modulated the simulated local field potential in agreement with physiological observations in humans. Intermediate levels of surround inhibition were also found to produce bistable coupling topologies that supported both waves and synchrony. State-dependent perturbation between bistable states produced very rapid transitions but were less reliable. We surmise that motor cortex may thus employ state-dependent computation to achieve very rapid changes between bistable motor states when the demand for speed exceeds the demand for accuracy.

Human Cortical Traveling Waves: Dynamical Properties and Correlations with Responses

The spatiotemporal behavior of human EEG oscillations is investigated. Traveling waves in the alpha and theta ranges are found to be common in both prestimulus and poststimulus EEG activity. The dynamical properties of these waves, including their speeds, directions, and durations, are systematically characterized for the first time, and the results show that there are significant changes of prestimulus spontaneous waves in the presence of an external stimulus. Furthermore, the functional relevance of these waves is examined by studying how they are correlated with reaction times on a single trial basis; prestimulus alpha waves traveling in the frontal-to-occipital direction are found to be most correlated to reaction speeds. These findings suggest that propagating waves of brain oscillations might be involved in mediating long-range interactions between widely distributed parts of human cortex.

Duration of Coherence Intervals in Electrical Brain Activity in Perceptual Organization

We investigated the relationship between visual experience and temporal intervals of synchronized brain activity. Using high-density scalp electroencephalography, we examined how synchronized activity depends on visual stimulus information and on individual observer sensitivity. In a perceptual grouping task, we varied the ambiguity of visual stimuli and estimated observer sensitivity to this variation. We found that durations of synchronized activity in the beta frequency band were associated with both stimulus ambiguity and sensitivity: the lower the stimulus ambiguity and the higher individual observer sensitivity the longer were the episodes of synchronized activity. Durations of synchronized activity intervals followed an extreme value distribution, indicating that they were limited by the slowest mechanism among the multiple neural mechanisms engaged in the perceptual task. Because the degree of stimulus ambiguity is (inversely) related to the amount of stimulus information, the durations of synchronous episodes reflect the amount of stimulus information processed in the task. We therefore interpreted our results as evidence that the alternating episodes of desynchronized and synchronized electrical brain activity reflect, respectively, the processing of information within local regions and the transfer of information across regions.

Fragmentation: loss of global coherence or breakdown of modularity in functional brain architecture?

Psychiatric illnesses characterized by disorganized cognition, such as schizophrenia, have been described in terms of fragmentation and hence understood as reduction in functional brain connectivity, particularly in prefrontal and parietal areas. However, as graph theory shows, relatively small numbers of nonlocal connections are sufficient to ensure global coherence in the modular small-world network structure of the brain. We reconsider fragmentation in this perspective. Computational studies have shown that for a given level of connectivity in a model of coupled nonlinear oscillators, modular small-world networks evolve from an initially random organization. Here we demonstrate that with decreasing connectivity, the probability of evolving into a modular small-world network breaks down at a critical point, which scales to the percolation function of random networks with a universal exponent of α = 1.17. Thus, according to the model, local modularity systematically breaks down before there is loss of global coherence in network connectivity. We, therefore, propose that fragmentation may involve, at least in its initial stages, the inability of a dynamically evolving network to sustain a modular small-world structure. The result is in a shift in the balance in schizophrenia from local to global functional connectivity.

Emergence of Complex Wave Patterns in Primate Cerebral Cortex

Slow brain rhythms are attributed to near-simultaneous (synchronous) changes in activity in neuron populations in the brain. Because they are slow and widespread, synchronous rhythms have not been considered crucial for information processing in the waking state. Here we adapted methods from turbulence physics to analyze δ-band (1–4 Hz) rhythms in local field potential (LFP) activity, in multielectrode recordings from cerebral cortex in anesthetized marmoset monkeys. We found that synchrony contributes only a small fraction (less than one-fourth) to the local spatiotemporal structure of δ-band signals. Rather, δ-band activity is dominated by propagating plane waves and spatiotemporal structures, which we call complex waves. Complex waves are manifest at submillimeter spatial scales, and millisecond-range temporal scales. We show that complex waves can be characterized by their relation to phase singularities within local nerve cell networks. We validate the biological relevance of complex waves by showing that nerve cell spike rates are higher in presence of complex waves than in the presence of synchrony and that there are nonrandom patterns of evolution from one type of complex wave to another. We conclude that slow brain rhythms predominantly indicate spatiotemporally organized activity in local nerve cell circuits, not synchronous activity within and across brain regions.

Propagating Waves Can Explain Irregular Neural Dynamics

Cortical neurons in vivo fire quite irregularly. Previous studies about the origin of such irregular neural dynamics have given rise to two major models: a balanced excitation and inhibition model, and a model of highly synchronized synaptic inputs. To elucidate the network mechanisms underlying synchronized synaptic inputs and account for irregular neural dynamics, we investigate a spatially extended, conductance-based spiking neural network model. We show that propagating wave patterns with complex dynamics emerge from the network model. These waves sweep past neurons, to which they provide highly synchronized synaptic inputs. On the other hand, these patterns only emerge from the network with balanced excitation and inhibition; our model therefore reconciles the two major models of irregular neural dynamics. We further demonstrate that the collective dynamics of propagating wave patterns provides a mechanistic explanation for a range of irregular neural dynamics, including the variability of spike timing, slow firing rate fluctuations, and correlated membrane potential fluctuations. In addition, in our model, the distributions of synaptic conductance and membrane potential are non-Gaussian, consistent with recent experimental data obtained using whole-cell recordings. Our work therefore relates the propagating waves that have been widely observed in the brain to irregular neural dynamics. These results demonstrate that neural firing activity, although appearing highly disordered at the single-neuron level, can form dynamical coherent structures, such as propagating waves at the population level.

Associative learning of classical conditioning as an emergent property of spatially extended spiking neural circuits with synaptic plasticity

Associative learning of temporally disparate events is of fundamental importance for perceptual and cognitive functions. Previous studies of the neural mechanisms of such association have been mainly focused on individual neurons or synapses, often with an assumption that there is persistent neural firing activity that decays slowly. However, experimental evidence supporting such firing activity for associative learning is still inconclusive. Here we present a novel, alternative account of associative learning in the context of classical conditioning, demonstrating that it is an emergent property of a spatially extended, spiking neural circuit with spike-timing dependent plasticity and short term synaptic depression. We show that both the conditioned and unconditioned stimuli can be represented by spike sequences which are produced by wave patterns propagating through the network, and that the interactions of these sequences are timing-dependent. After training, the occurrence of the sequence encoding the conditioned stimulus (CS) naturally regenerates that encoding the unconditioned stimulus (US), therefore resulting in association between them. Such associative learning based on interactions of spike sequences can happen even when the timescale of their separation is significantly larger than that of individual neurons. In particular, our network model is able to account for the temporal contiguity property of classical conditioning, as observed in behavioral studies. We further show that this emergent associative learning in our network model is quite robust to noise perturbations. Our results therefore demonstrate that associative learning of temporally disparate events can happen in a distributed way at the level of neural circuits.

The rhythms of steady posture

Beta-band (15-30Hz) oscillations in motor cortex have been implicated in voluntary movement and postural control. Yet the mechanisms linking those oscillations to function remains elusive. Recently, spatial waves of synchronized beta oscillations have been observed in primary and pre-motor cortex during delayed-reaching movements. Here we propose that the motor cortex may exploit differences in the morphological properties of spatial oscillation patterns to encode motor commands. Furthermore, we argue that the descending motor pathways spatially filter those patterns to selectively shape the motor drive to the muscles. The ensuing motor drive need not be overtly rhythmic despite the oscillatory nature of the neural coding scheme. We demonstrate this principle using a model of the descending motor system in which oscillatory cortical patterns govern steady postures in a simulated biomechanical joint. The cortex was represented by a sheet of coupled oscillators operating in the beta-band. Lateral inhibition between the oscillators induced spatially synchronized beta waves. The spatial orientation of those waves was governed by the dominant direction of lateral inhibition, which we manipulated. The descending motor tracts that emanated from the cortex were tuned such that specific muscles responded selectively to cortical waves with a given orientation. A range of steady joint postures could thus be achieved by manipulating the dominant direction of the lateral coupling. The model thereby demonstrates the proposed mechanism by which oscillatory patterns in cortex are translated into steady motor postures. The model also reproduces some oscillatory aspects of motor physiology. In particular, it replicates the general reduction of cortical beta power at the onset of movement and the weak but significant levels of corticomuscular coherence observed during steady motor output. HighlightsWe propose a functional role for spatially organized oscillations in motor cortex.Motor commands are encoded in the morphology of spatial oscillation patterns.A neural mechanism for translating those patterns into motor drive is presented.Steady motor drives are maintained for the lifetime of the oscillation patterns.The mechanism also reproduces physiological aspects of corticomuscular coherence.