# Fast Response and Temporal Coding on Coherent Oscillations in Small-World Networks

## Abstract

We have investigated the role that different connectivity regimes play on the dynamics of a network of Hodgkin-Huxley neurons by computer simulations. The different connectivity topologies exhibit the following features: random connectivity topologies give rise to fast system response yet are unable to produce coherent oscillations in the average activity of the network; on the other hand, regular connectivity topologies give rise to coherent oscillations and temporal coding, but in a temporal scale that is not in accordance with fast signal processing. Finally, small-world (SW) connectivity topologies, which fall between random and regular ones, take advantage of the best features of both, giving rise to fast system response with coherent oscillations along with reproducible temporal coding on clusters of neurons. Our work is the first, to the best of our knowledge, to show the need for a small-world topology in order to obtain all these features in synergy within a biologically plausible time scale.

In a recent letter by Watts and Strogatz  it was shown that small-world networks enhance signal-propagation speed, computational power, and synchronizability. Small-world stands for a network whose connectivity topology is placed somewhere between a regular and a completely random connectivity. The main properties of these specific networks are that they can be highly clustered like regular networks and, at the same time, have small path lengths like random ones. Therefore, small-world networks may have properties given neither in regular nor in random networks .

In this letter we have extended Watts and Strogatz’s general framework by introducing dynamical elements in the network nodes. Our source of inspiration is based on a phenomena observed in the olfactory antennal lobe (AL) of the locust discovered by Gilles Laurent and collaborators . The AL is a group of around 800 neurons whose functional role is to relay information from the olfactory receptors to higher areas of the brain for further processing. Three main features have been observed in the dynamics of the AL. First, there is a fast response of the AL when the stimulus is presented. Second, when an odour is presented to the insect, coherent oscillations of 20 Hz in the local field potential (LFP) are measured . Third, every neuron responds to the odour with some particular timing with respect to the LFP . Summarizing: fast response of coherent oscillations along with temporal coding are observed. There are also other systems in the brain that present coherent LFP oscillations, hence, hinting to the generality of these phenomena (see  for a review).

The cooperative behavior of large assemblies of dynamical elements has been the subject of many investigations. In all of them the connectivity between the elements of the network was either regular (local or global all-to-all), or random. However, none of these studies incorporates a comparative analysis of network dynamics for all the different connectivity topologies.

In the present work we pretend to show that in order to provide fast response, coherent oscillations and temporal coding a small-world topology is required. We will show that the regular connectivity topology provides a slow response to the external input. Although it is able to produce temporal coding and coherent oscillations, the time of formation of the oscillations would imply much slower responses than those observed in biological systems. On the other hand, for the completely random connectivity case the responsiveness of the system is highly increased and temporal variations in clusters activity are present, but the coherent oscillations tipically observed in the LFP are lost. Without these coherent oscillations the AL seems to lose its ability to process the information incoming from the sensors .

The model we propose for this study is made of an array of non-identical Hodgkin-Huxley elements coupled by excitatory synapses. The unit dynamics is described by the following set of coupled ordinary differential equations:

$$C_m\dot{V}_i=I^e(t)g_L\widehat{V}_Lg_{Na}m^3h\widehat{V}_{Na}g_Kn^4\widehat{V}_K+I^s(t)$$
(1)   
$$\dot{m}=\alpha _m(V)(1m)\beta _m(V)m$$
(3)   
$$\dot{h}=\alpha _h(V)(1h)\beta _h(V)h$$
(4)   
$$\dot{n}=\alpha _n(V)(1n)\beta _n(V)n$$
(5)   
where $`V_i`$ represents the membrane potential of unit $`i`$; $`C_m`$ is the membrane capacitance per unit area; $`I^e(t)`$ is the external current, which occurs as a pulse of amplitude $`I_0`$; $`I^s(t)`$ is the synaptic current; $`\widehat{V}_r=V_iV_r`$, where $`V_r`$ are the equilibrium potentials for the different ionic contributions ($`r=L,Na,K`$), and $`g_r`$ are the corresponding maximum conductances per unit area; $`h`$, $`m`$, $`n`$ are the voltage dependent conductances; and $`\alpha `$, $`\beta `$ are functions of $`V`$ adjusted to physiological data by voltage clamp techniques. We have used the original functions and parameters employed by Hodgkin and Huxley .

The system was integrated using the Runge-Kutta 6(5) scheme with variable time step based on . The absolute error was $`10^{15}`$ and the relative error was $`10^7`$ in all the calculations presented in this letter. The synaptic current $`I^s`$ is given by

$$I_i^s(t)=g_{ij}r_j(t)[V_s(t)E_s]$$
(6)   
where $`i`$ stands for the index of the neuron that receives the synaptic input, $`j`$ is the neuron from which the synaptic input is received, and $`g_{ij}`$ is the maximum conductance, which determines the degree of coupling between the two connected neurons. $`V_s`$ is the postsynaptic potential, $`E_s`$ is the synaptic reversal potential and $`r_j(t)`$ is the fraction of bound receptors computed following the method and parameters described by Destexhe et al. . Namely, the dynamics of the bound receptors $`r`$ is given by the equation:

$$\dot{r}=\alpha [T](1r)\beta r$$
(7)   
where $`[T]`$ is the concentration of the transmitter, and $`\alpha `$, $`\beta `$ are the rise and decay constants, respectively.

In this model three different kinds of connectivity patterns have been tested: regular, random and small world. To interpolate between regular and random networks we follow the procedure described by Watts and Strogatz  which we summarize here for convenience: we start from a ring lattice with $`N`$ vertices and $`k`$ edges per vertex, and each edge is rewired at random with probability $`p`$. The limits of regularity and randomness are for $`p=0`$ and $`p=1`$ respectively, and the small-world topology lies somewhere in the intermediate region $`0<p<1`$. The quantification of the structural properties of these graphs is performed, following Watts and Strogatz , using their characteristic path length $`L(p)`$ and their clustering coefficient $`C(p)`$. $`L(p)`$ is defined as the number of edges in the shortest path between two vertices, averaged over all pairs of vertices. $`C(p)`$ is defined as follows: suppose that a vertex $`v`$ has $`k_v`$ neighbours; then at most $`k_v(k_v1)/2`$ edges can exist between them. Let $`C_v`$ denote the fraction of these allowable edges that actually exist, and define $`C`$ as the average of $`C_v`$ over all vertices $`v`$. Fig. 1a replicates that of Watts and Strogatz  for ease of reference and to verify our computations.

Next we investigate the functional significance of SW topologies for the dynamics of the network. Watts and Strogatz  already note that small-world networks of coupled phase oscillators synchronize almost as readily as in the mean-field model, despite having orders of magnitude fewer edges. To study the global behavior of the network we compute its average activity $`\overline{V(t)}=(1/N)_{i=1}^NV_i(t)`$. The quantity that we use to detect the onset and degree of coherent oscillations is the average activity oscillation amplitude , defined by

$$\sigma ^2(p)=\frac{1}{T_2T_1}_{T_1}^{T_2}[\overline{V_p(t)}_t\overline{V_p(t)}]^2𝑑t$$
(8)   
where $`\overline{V_p(t)}`$ is the average activity of the network for a given value of the probability $`p`$, and the angle brackets denote temporal average over the integration interval. A high value of $`\sigma (p)`$ would imply a high amplitude of the oscillations of the average activity, while a low value would indicate an almost non-oscillatory behavior. In Fig. 1b we plot $`\sigma (p)`$ for each of the different networks characterized by its probability p. Notice that coherent oscillations increase in the region in which a high $`C(p)`$ and a low $`L(p)`$ occur simultaneously; this is precisely the SW region. This can be better observed in Fig. 2, which shows the average activity of the network in three cases corresponding to the three different topological configurations: regular, random and SW. Both the regular and the SW topologies display coherent oscillations, but in the regular network they appear much later and their amplitude is smaller than in the SW case. On the other hand, the random network only displays irregular variations over an almost constant pattern of activity.

A more extensive study in the $`(k,p)`$ plane has been performed in order to stablish the limits for the appearance of coherent oscillations and to check that our previous results can be generalized within a certain range of parameters. We have computed the average activity oscillation amplitude for a total of $`180`$ points in the $`(k,p)`$ plane, taking an integration interval between $`T_1=100`$ and $`T_2=200`$. An interpolation of these results is plotted in Fig. 3, where the clear zones indicate high values of $`\sigma `$. We can conclude from this figure that fast coherent oscillations appear only in the region of intermediate probabilities, that is, the SW. The a priori limits on $`k`$ are based on the fact that for $`k`$ lower than $`10`$ the activation of the network is very weak, while for $`k`$ higher than $`35`$ some neurons become saturated.

Having shown the necessity of a SW network to obtain a fast response along with coherent oscillations of the average activity, we proceed to check the ability of the network to produce a temporal codification of the information contained in the stimulus, and the robustness of the network response to the introduction of noise in the input.

In temporal coding, information is represented by the timing of action potentials with respect to an ongoing collective oscillatory pattern of activity. For instance, when an odour is presented, every neuron in the AL responds to the odour with some particular timing with respect to the LFP . As a measure of this temporal coding, we have divided time in periods of the global average activity, and calculated for each period the quantity:

$$A_i(n)=\frac{1}{C}_T[a_i(t)\overline{V(t)}]^2𝑑t$$
(9)   
where $`i`$ represents a particular cluster, $`n`$ a particular period of the mean activity $`\overline{V(t)}`$ of the whole network, $`a_i(t)`$ is the mean activity of cluster $`i`$, and $`C`$ is an appropiate normalization constant used to get the final value of $`A_i(n)`$ in the range $`01`$.

We would expect the coding to be different for each cluster. In Fig. 4 we show the results for three different clusters chosen at random in a network within the SW connectivity regime. It can be observed that the activities of the different clusters are out of phase and reach their maximum values at different periods of the global average activity.

A system with such a coding can rapidly and efficiently perform computations that are essential to pattern recognition, and that are much more difficult to perform in a rate-coding framework . Following this coding scheme, information about an odour is contained not only in the neural assembly active at each oscillation cycle, but also in the precise temporal sequence in which these assemblies are updated during the response to the odour. Temporal coding thus allows combinatorial representations in time as well as in space .

Lastly, in order to check the robustness of the network response, we have computed correlations between the activities of a given cluster in five different realizations of the simulation. We have introduced a gaussian uncorrelated noise to the external input: $`I^e=I_0+\sigma ϵ`$, where $`\sigma `$ is the outcome of a normal distibution and $`ϵ`$ is the noise level. The correlations are calculated as follows:

$$C_i^{(rs)}(ϵ)=\frac{_nm_i^{(r)}(n)m_i^{(s)}(n)}{\sqrt{_nm_i^{(r)}(n)^2_nm_i^{(s)}(n)^2}}$$
(10)   
where $`r`$ and $`s`$ correspond to different realizations of the simulation, $`i`$ is the cluster, the sums are over all periods $`n`$, and the dependence on the noise is implicit in the right side of the equation. We have defined the quantity $`m_i^{(r)}(n)=A_i^{(r)}(n)A_i^{(r)}`$, with $`A_i^{(r)}(n)`$ the magnitude from Eq. (9), for a particular realization $`r`$. The angle brackets denote average over all periods $`n`$.

An average of the correlation curves for different pairs of realizations is plotted in Fig. 5. There are two clearly different regions in the graphic: for small amounts of noise the correlation is almost $`1.0`$; whereas for a higher noise level the correlation jumps to a lower value. The discontinuity appears at a level of noise of approximately $`0.1`$ percent.

In conclusion, a variety of possible network topologies has been investigated. Each one gives rise to different dynamical properties. Regular networks produce coherent oscillations and temporal coding in a slow time scale; whereas random networks give rise to fast response but without coherent oscillations. We have introduced new results on small-world networks, showing that both coherent oscillations and temporal coding can coexist in synergy in a fast time scale. At the onset of this research project, intrigued by the olfactory AL dynamics, we were searching for a dynamical system with precisely the properties just described for the SW networks. Hence the work here reported is not only interesting from the dynamical systems point of view, but it is also relevant for the understanding of biological systems.

We want to acknowledge Gilles Laurent, Alex Bäcker, Maxim Bazhenov, Misha Rabinovich and Henry Abarbanel for very insightful discusions. We thank the Dirección General de Enseñanza Superior e Investigación Científica for financial support (PB97-1448). We thank the Universidad Autónoma de Madrid for a graduate fellowship to L. F. L. and the Centro de Computación Científica (UAM) for the computation time.