Fast Synchronization of Perpetual Grouping in Laminar Visual Cortical Circuits

Perceptual grouping is well-known to be a fundamental process during visual perception, notably grouping across scenic regions that do not receive contrastive visual inputs. Illusory contours are a classical example of such groupings. Recent psychophysical and neurophysiological evidence have shown that the grouping process can facilitate rapid synchronization of the cells that are bound together by a grouping, even when the grouping must be completed across regions that receive no contrastive inputs. Synchronous grouping can hereby bind together different object parts that may have become desynchronized due to a variety of factors, and can enhance the efficiency of cortical transmission. Neural models of perceptual grouping have clarified how such fast synchronization may occur by using bipole grouping cells, whose predicted properties have been supported by psychophysical, anatomical, and neurophysiological experiments. These models have not, however, incorporated some of the realistic constraints on which groupings in the brain are conditioned, notably the measured spatial extent of long-range interactions in layer 2/3 of a grouping network, and realistic synaptic and axonal signaling delays within and across cells in different cortical layers. This work addresses the question: Can long-range interactions that obey the bipole constraint achieve fast synchronization under realistic anatomical and neurophysiological constraints that initially desynchronize grouping signals? Can the cells that synchronize retain their analog sensitivity to changing input amplitudes? Can the grouping process complete and synchronize illusory contours across gaps in bottom-up inputs? Our simulations show that the answer to these questions is Yes.Office of Naval Research (N00014-01-1-0624); Air Force Office of Scientific Research (F49620-01-1-03097

Attentional modulation of firing rate and synchrony in a model cortical network

When attention is directed into the receptive field of a V4 neuron, its contrast response curve is shifted to lower contrast values (Reynolds et al, 2000, Neuron 26:703). Attention also increases the coherence between neurons responding to the same stimulus (Fries et al, 2001, Science 291:1560). We studied how the firing rate and synchrony of a densely interconnected cortical network varied with contrast and how they were modulated by attention. We found that an increased driving current to the excitatory neurons increased the overall firing rate of the network, whereas variation of the driving current to inhibitory neurons modulated the synchrony of the network. We explain the synchrony modulation in terms of a locking phenomenon during which the ratio of excitatory to inhibitory firing rates is approximately constant for a range of driving current values. We explored the hypothesis that contrast is represented primarily as a drive to the excitatory neurons, whereas attention corresponds to a reduction in driving current to the inhibitory neurons. Using this hypothesis, the model reproduces the following experimental observations: (1) the firing rate of the excitatory neurons increases with contrast; (2) for high contrast stimuli, the firing rate saturates and the network synchronizes; (3) attention shifts the contrast response curve to lower contrast values; (4) attention leads to stronger synchronization that starts at a lower value of the contrast compared with the attend-away condition. In addition, it predicts that attention increases the delay between the inhibitory and excitatory synchronous volleys produced by the network, allowing the stimulus to recruit more downstream neurons.Comment: 36 pages, submitted to Journal of Computational Neuroscienc

Dynamical Mean Field approximation of a canonical cortical model for studying inter-population synchrony

The goal of this paper is twofold. We propose and explore a model to study the synchronization among populations in the canonical model of the neocortex proposed previously by (R.J. Douglas, K.A.C. Martin, A functional microcircuit for cat visual cortex. J.Physiol. 440(1991) 735–769). For this, a model describing N synapses of each m-population (m = 1, 2,3) is proposed. Each synapse is described by a system of 2 stochastic differential equations (SDEs). Then, by using the dynamical mean field approximation (DMA) (H. Hasegawa, Dynamical mean-field theory of spiking neuron ensembles: Response to a single spike with independent noises, Phys. Rev. E. (2003)1-19.) the system of several SDEs is reduced to 12 ordinary differential equations for the means and the second-order moments of global variables. The connectivity among populations is obtained by summarizing in the canonical model the detailed information from a quantitative description of the circuits formed in cat area 17 given in (T.Binzegger, R.J. Douglas, K.A. Martin, A Quantitative Map of the Circuit of Cat Primary Visual Cortex, J. Neurosci. 24 (2004) 8441- 8453). In the framework of the used DMA we propose a measure for inter-population synchronization. Simulations are carried out for exploring how inter-population synchrony is related to the variation of firing frequency of each population. Our results suggest that superficial pyramidal clusters appear to have a predominant influence on the synchronization process among pyramidal populations as well as put forward the active role of inhibition in the rest of the synchronizations between populations

Phase locking in networks of synaptically coupled McKean relaxation oscillators

We use geometric dynamical systems methods to derive phase equations for networks of weakly connected McKean relaxation oscillators. We derive an explicit formula for the connection function when the oscillators are coupled with chemical synapses modeled as the convolution of some input spike train with an appropriate synaptic kernel. The theory allows the systematic investigation of the way in which a slow recovery variable can interact with synaptic time scales to produce phase-locked solutions in networks of pulse coupled neural relaxation oscillators. The theory is exact in the singular limit that the fast and slow time scales of the neural oscillator become effectively independent. By focusing on a pair of mutually coupled McKean oscillators with alpha function synaptic kernels, we clarify the role that fast and slow synapses of excitatory and inhibitory type can play in producing stable phase-locked rhythms. In particular we show that for fast excitatory synapses there is coexistence of a stable synchronous, a stable anti-synchronous, and one stable asynchronous solution. For slower synapses the anti-synchronous solution can lose stability, whilst for even slower synapses it can regain stability. The case of inhibitory synapses is similar up to a reversal of the stability of solution branches. Using a return-map analysis the case of strong pulsatile coupling is also considered. In this case it is shown that the synchronous solution can co-exist with a continuum of asynchronous states

Simulations of Neocortical Columnar Oscillations

The intentionof this thesis is to examine the role of the neocortical local drcuit in supporting synchronisatLon and fast (gamma) oscUlation. The aim is to include stereotypical features of the local neocortex in model simulations of cortical activity. Modelling is hmitedby scale in number and detail. Model features include three neurontypes(RS, FS and IB) andsynapses with three time courses takenfrom reportedtri-phasic PSPs (fEPSP, flPSP andsIPSP). Cell types and synapses are distributedin a two layer model. The contribution of the layers to columnactivity is investigated. The upperlayer has a tendancy towardspredse synchronisation and can dominate the activity producing synchronisation and oscillation in the whole column. This is attributed to the stronger inhibitory circuit in the upperlayer. The lower layer achieves a less precise synchronisatiorv this is attributed to a lower level of inhibition and the intraburst duration of IB neurons. The significance of this difference in the temporal properties of the two layers is discussed in relation to existing theories andmodels of local cortical function. Following a further consideration of local cortical physiology a new model of cortical functioning is proposed. The key features of this model include: the generation of local oscillations in a vertical interlarninar reciprocal circuit; the apical dendrite providing a sharp coincidence detection functionbetweenthe layers; slow axonal lateral propagationprovidinga time delay network; apical dendrites of bursting cells (CH and IB) providing coincidence detectionbetweenmputs 6:0m distant areas (layer 1 inputs) and local activity; bursting cell innervationof intemeurons, linking the local oscillation cy de to coinddence detection. This moddis termed an'intrinsically osdllating time coding networld (lOTCN). Specific predictions are made concerning the functiorungof the local circuit m neocortex, and the connectivity of CH neurons

Inhibitory synchrony as a mechanism for attentional gain modulation

Recordings from area V4 of monkeys have revealed that when the focus of attention is on a visual stimulus within the receptive field of a cortical neuron, two distinct changes can occur: The firing rate of the neuron can change and there can be an increase in the coherence between spikes and the local field potential in the gamma-frequency range (30-50 Hz). The hypothesis explored here is that these observed effects of attention could be a consequence of changes in the synchrony of local interneuron networks. We performed computer simulations of a Hodgkin-Huxley type neuron driven by a constant depolarizing current, I, representing visual stimulation and a modulatory inhibitory input representing the effects of attention via local interneuron networks. We observed that the neuron's firing rate and the coherence of its output spike train with the synaptic inputs was modulated by the degree of synchrony of the inhibitory inputs. The model suggest that the observed changes in firing rate and coherence of neurons in the visual cortex could be controlled by top-down inputs that regulated the coherence in the activity of a local inhibitory network discharging at gamma frequencies.Comment: J.Physiology (Paris) in press, 11 figure

Evolutionary game theory and the evolution of neuron populations, ring rates, and decisionmaking

Ours, is the first application of dynamical evolutionary games to decision making in neuroscience. Firing neurons are the players. The strategy is their firing rate. Neurons with equal firing rates define a population. The neurons do not know the rules of the game, they do not know what the reward is, they are not required to be rational and they do not even know they are playing the game. Interactions are inhibitory. The theory confirms experimental data about decision making in vision: (i ) A parameter of the game model determines how many populations of neurons participate in the decision; (ii ) the solution of the game dictates how many loci in the brain participate in the decision; (iii ) the theory clarifies the difference between ultimate and proximate factors and predicts that quick decisions are associated with more errors and slow decision are associated with fewer errors

Criteria on Balance, Stability, and Excitability in Cortical Networks for Constraining Computational Models

During ongoing and Up state activity, cortical circuits manifest a set of dynamical features that are conserved across these states. The present work systematizes these phenomena by three notions: excitability, the ability to sustain activity without external input; balance, precise coordination of excitatory and inhibitory neuronal inputs; and stability, maintenance of activity at a steady level. Slice preparations exhibiting Up states demonstrate that balanced activity can be maintained by small local circuits. While computational models of cortical circuits have included different combinations of excitability, balance, and stability, they have done so without a systematic quantitative comparison with experimental data. Our study provides quantitative criteria for this purpose, by analyzing in-vitro and in-vivo neuronal activity and characterizing the dynamics on the neuronal and population levels. The criteria are defined with a tolerance that allows for differences between experiments, yet are sufficient to capture commonalities between persistently depolarized cortical network states and to help validate computational models of cortex. As test cases for the derived set of criteria, we analyze three widely used models of cortical circuits and find that each model possesses some of the experimentally observed features, but none satisfies all criteria simultaneously, showing that the criteria are able to identify weak spots in computational models. The criteria described here form a starting point for the systematic validation of cortical neuronal network models, which will help improve the reliability of future models, and render them better building blocks for larger models of the brain

Neural models of learning and visual grouping in the presence of finite conduction velocities

The hypothesis of object binding-by-synchronization in the visual cortex has been supported by recent experiments in awake monkeys. They demonstrated coherence among gamma-activities (30–90 Hz) of local neural groups and its perceptual modulation according to the rules of figure-ground segregation. Interactions within and between these neural groups are based on axonal spike conduction with finite velocities. Physiological studies confirmed that the majority of transmission delays is comparable to the temporal scale defined by gamma-activity (11–33 ms). How do these finite velocities influence the development of synaptic connections within and between visual areas? What is the relationship between the range of gamma-coherence and the velocity of signal transmission? Are these large temporal delays compatible with recently discovered phenomenon of gamma-waves traveling across larger parts of the primary visual cortex? The refinement of connections in the immature visual cortex depends on temporal Hebbian learning to adjust synaptic efficacies between spiking neurons. The impact of constant, finite, axonal spike conduction velocities on this process was investigated using a set of topographic network models. Random spike trains with a confined temporal correlation width mimicked cortical activity before visual experience. After learning, the lateral connectivity within one network layer became spatially restricted, the width of the connection profile being directly proportional to the lateral conduction velocity. Furthermore, restricted feedforward divergence developed between neurons of two successive layers. The size of this connection profile matched the lateral connection profile of the lower layer neuron. The mechanism in this network model is suitable to explain the emergence of larger receptive fields at higher visual areas while preserving a retinotopic mapping. The influence of finite conduction velocities on the local generation of gamma-activities and their spatial synchronization was investigated in a model of a mature visual area. Sustained input and local inhibitory feedback was sufficient for the emergence of coherent gamma-activity that extended across few millimeters. Conduction velocities had a direct impact on the frequency of gamma-oscillations, but did neither affect gamma-power nor the spatial extent of gamma-coherence. Adding long-range horizontal connections between excitatory neurons, as found in layer 2/3 of the primary visual cortex, increased the spatial range of gamma-coherence. The range was maximal for zero transmission delays, and for all distances attenuated with finite, decreasing lateral conduction velocities. Below a velocity of 0.5 m/s, gamma-power and gamma-coherence were even smaller than without these connections at all, i.e., slow horizontal connections actively desynchronized neural populations. In conclusion, the enhancement of gamma-coherence by horizontal excitatory connections critically depends on fast conduction velocities. Coherent gamma-activity in the primary visual cortex and the accompanying models was found to only cover small regions of the visual field. This challenges the role of gamma-synchronization to solve the binding problem for larger object representations. Further analysis of the previous model revealed that the patches of coherent gamma-activity (1.8 mm half-height decline) were part of more globally occurring gamma-waves, which coupled over much larger distances (6.3 mm half-height decline). The model gamma-waves observed here are very similar to those found in the primary visual cortex of awake monkeys, indicating that local recurrent inhibition and restricted horizontal connections with finite axonal velocities are sufficient requirements for their emergence. In conclusion, since the model is in accordance with the connectivity and gamma-processes in the primary visual cortex, the results support the hypothesis that gamma-waves provide a generalized concept for object binding in the visual cortex