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Register a new userMaximum entropy models reveal the excitatory and inhibitory correlation structures in cortical neuronal activity
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Maximum Entropy models can be inferred from large data-sets to uncover how collective dynamics emerge from local interactions. Here, such models are employed to investigate neurons recorded by multielectrode arrays in the human and monkey cortex. Taking advantage of the separation of excitatory and inhibitory neuron types, we construct a model including this distinction. This approach allows to shed light upon differences between excitatory and inhibitory activity across different brain states such as wakefulness and deep sleep, in agreement with previous findings. Additionally, Maximum Entropy models can also unveil novel features of neuronal interactions, which are found to be dominated by pairwise interactions during wakefulness, but are population-wide during deep sleep. In particular, inhibitory neurons are observed to be strongly tuned to the inhibitory population. Overall, we demonstrate Maximum Entropy models can be useful to analyze data-sets with classified neuron types, and to reveal the respective roles of excitatory and inhibitory neurons in organizing coherent dynamics in the cerebral cortex.
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It is widely appreciated that well-balanced excitation and inhibition are necessary for proper function in neural networks. However, in principle, such balance could be achieved by many possible configurations of excitatory and inhibitory strengths, and relative numbers of excitatory and inhibitory neurons. For instance, a given level of excitation could be balanced by either numerous inhibitory neurons with weak synapses, or few inhibitory neurons with strong synapses. Among the continuum of different but balanced configurations, why should any particular configuration be favored? Here we address this question in the context of the entropy of network dynamics by studying an analytically tractable network of binary neurons. We find that entropy is highest at the boundary between excitation-dominant and inhibition-dominant regimes. Entropy also varies along this boundary with a trade-off between high and robust entropy: weak synapse strengths yield high network entropy which is fragile to parameter variations, while strong synapse strengths yield a lower, but more robust, network entropy. In the case where inhibitory and excitatory synapses are constrained to have similar strength, we find that a small, but non-zero fraction of inhibitory neurons, like that seen in mammalian cortex, results in robust and relatively high entropy.
In this paper, we clarify the mechanisms underlying a general phenomenon present in pulse-coupled heterogeneous inhibitory networks: inhibition can induce not only suppression of the neural activity, as expected, but it can also promote neural reactivation. In particular, for globally coupled systems, the number of firing neurons monotonically reduces upon increasing the strength of inhibition (neurons death). However, the random pruning of the connections is able to reverse the action of inhibition, i.e. in a sparse network a sufficiently strong synaptic strength can surprisingly promote, rather than depress, the activity of the neurons (neurons rebirth). Thus the number of firing neurons reveals a minimum at some intermediate synaptic strength. We show that this minimum signals a transition from a regime dominated by the neurons with higher firing activity to a phase where all neurons are effectively sub-threshold and their irregular firing is driven by current fluctuations. We explain the origin of the transition by deriving an analytic mean field formulation of the problem able to provide the fraction of active neurons as well as the first two moments of their firing statistics. The introduction of a synaptic time scale does not modify the main aspects of the reported phenomenon. However, for sufficiently slow synapses the transition becomes dramatic, the system passes from a perfectly regular evolution to an irregular bursting dynamics. In this latter regime the model provides predictions consistent with experimental findings for a specific class of neurons, namely the medium spiny neurons in the striatum.
Dynamic excitatory-inhibitory (E-I) balance is a paradigmatic mechanism invoked to explain the irregular low firing activity observed in the cortex. However, we will show that the E-I balance can be at the origin of other regimes observable in the brain. The analysis is performed by combining simulations of sparse E-I networks composed of N spiking neurons with analytical investigations of low dimensional neural mass models. The bifurcation diagrams, derived for the neural mass model, allow to classify the asynchronous and coherent behaviours emerging any finite in-degree K. In the limit N >> K >> 1 both supra and sub-threshold balanced asynchronous regimes can be observed. Due to structural heterogeneity the asynchronous states are characterized by the splitting of the neurons in three groups: silent, fluctuation and mean driven. The coherent rhythms are characterized by regular or irregular temporal fluctuations joined to spatial coherence similar to coherent fluctuations observed in the cortex over multiple spatial scales. Collective Oscillations (COs) can emerge due to two different mechanisms. A first mechanism similar to the pyramidal-interneuron gamma (PING) one. The second mechanism is intimately related to the presence of current fluctuations, which sustain COs characterized by an essentially simultaneous bursting of the two populations. We observe period-doubling cascades involving the PING-like COs finally leading to the appearance of coherent chaos. For sufficiently strong current fluctuations we report a novel mechanism of frequency locking among collective rhythms promoted by these intrinsic fluctuations. Our analysis suggest that despite PING-like or fluctuation driven COS are observable for any finite in-degree K, in the limit N >> K >> 1 these solutions result in two coexisting balanced regimes: an asynchronous and a fully synchronized one.
Experimental and numerical results suggest that the brain can be viewed as a system acting close to a critical point, as confirmed by scale-free distributions of relevant quantities in a variety of different systems and models. Less attention has received the investigation of the temporal correlation functions in brain activity in different, healthy and pathological, conditions. Here we perform this analysis by means of a model with short and long-term plasticity which implements the novel feature of different recovery rates for excitatory and inhibitory neurons, found experimentally. We evidence the important role played by inhibitory neurons in the supercritical state: We detect an unexpected oscillatory behaviour of the correlation decay, whose frequency depends on the fraction of inhibitory neurons and their connectivity degree. This behaviour can be rationalized by the observation that bursts in activity become more frequent and with a smaller amplitude as inhibition becomes more relevant.
A companion paper introduces a nonlinear network with Hebbian excitatory (E) neurons that are reciprocally coupled with anti-Hebbian inhibitory (I) neurons and also receive Hebbian feedforward excitation from sensory (S) afferents. The present paper derives the network from two normative principles that are mathematically equivalent but conceptually different. The first principle formulates unsupervised learning as a constrained optimization problem: maximization of S-E correlations subject to a copositivity constraint on E-E correlations. A combination of Legendre and Lagrangian duality yields a zero-sum continuous game between excitatory and inhibitory connections that is solved by the neural network. The second principle defines a zero-sum game between E and I cells. E cells want to maximize S-E correlations and minimize E-I correlations, while I cells want to maximize I-E correlations and minimize power. The conflict between I and E objectives effectively forces the E cells to decorrelate from each other, although only incompletely. Legendre duality yields the neural network.
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