Yasuhiro Tsubo

Made-to-order spiking neuron model equipped with a multi-timescale adaptive threshold

Information is transmitted in the brain through various kinds of neurons that respond differently to the same signal. Full characteristics including cognitive functions of the brain should ultimately be comprehended by building simulators capable of precisely mirroring spike responses of a variety of neurons. Neuronal modeling that had remained on a qualitative level has recently advanced to a quantitative level, but is still incapable of accurately predicting biological data and requires high computational cost. In this study, we devised a simple, fast computational model that can be tailored to any cortical neuron not only for reproducing but also for predicting a variety of spike responses to greatly fluctuating currents. The key features of this model are a multi-timescale adaptive threshold predictor and a nonresetting leaky integrator. This model is capable of reproducing a rich variety of neuronal spike responses, including regular spiking, intrinsic bursting, fast spiking, and chattering, by adjusting only three adaptive threshold parameters. This model can express a continuous variety of the firing characteristics in a three-dimensional parameter space rather than just those identified in the conventional discrete categorization. Both high flexibility and low computational cost would help to model the real brain function faithfully and examine how network properties may be influenced by the distributed characteristics of component neurons.

Optimal spike-based communication in excitable networks with strong-sparse and weak-dense links

The connectivity of complex networks and functional implications has been attracting much interest in many physical, biological and social systems. However, the significance of the weight distributions of network links remains largely unknown except for uniformly- or Gaussian-weighted links. Here, we show analytically and numerically, that recurrent neural networks can robustly generate internal noise optimal for spike transmission between neurons with the help of a long-tailed distribution in the weights of recurrent connections. The structure of spontaneous activity in such networks involves weak-dense connections that redistribute excitatory activity over the network as noise sources to optimally enhance the responses of individual neurons to input at sparse-strong connections, thus opening multiple signal transmission pathways. Electrophysiological experiments confirm the importance of a highly broad connectivity spectrum supported by the model. Our results identify a simple network mechanism for internal noise generation by highly inhomogeneous connection strengths supporting both stability and optimal communication.

Layer and frequency dependencies of phase response properties of pyramidal neurons in rat motor cortex.

It is postulated that synchronous firing of cortical neurons plays an active role in cognitive functions of the brain. An important issue is whether pyramidal neurons in different cortical layers exhibit similar tendencies to synchronise. To address this issue, we performed intracellular and whole‐cell recordings of regular‐spiking pyramidal neurons in slice preparations of the rat motor cortex (18–45 days old) and analysed the phase response curves of these pyramidal neurons in layers 2/3 and 5. The phase response curve represents how an external stimulus affects the timing of spikes immediately after the stimulus in repetitively firing neurons. The phase response curve can be classified into two categories, type 1 (the spike is always advanced) and type 2 (the spike is advanced or delayed depending on the stimulus phase), and are important determinants of whether or not rhythmic synchronization of neuron pairs occurs. We found that pyramidal neurons in layer 2/3 tend to display type‐2 phase response curves whereas those in layer 5 tend to exhibit type‐1 phase response curves. The differences were prominent particularly in the gamma‐frequency range (20–45 Hz). Our results imply that the layer‐2/3 pyramidal neurons, when coupled mutually through fast excitatory synapses, may exhibit a much stronger tendency for rhythmic synchronization than layer‐5 neurons in the gamma‐frequency range.

Synchrony of limit-cycle oscillators induced by random external impulses

The mechanism of phase synchronization between uncoupled limit-cycle oscillators induced by common external impulsive forcing is analyzed. By reducing the dynamics of the oscillator to a random phase map, it is shown that phase synchronization generally occurs when the oscillator is driven by weak external impulses in the limit of large inter-impulse intervals. The case where the inter-impulse intervals are finite is also analyzed perturbatively for small impulse intensity. For weak Poissonian impulses, it is shown that the phase synchronization persists up to the first order approximation.

Balanced Excitatory and Inhibitory Inputs to Cortical Neurons Decouple Firing Irregularity from Rate Modulations

In vivo cortical neurons are known to exhibit highly irregular spike patterns. Because the intervals between successive spikes fluctuate greatly, irregular neuronal firing makes it difficult to estimate instantaneous firing rates accurately. If, however, the irregularity of spike timing is decoupled from rate modulations, the estimate of firing rate can be improved. Here, we introduce a novel coding scheme to make the firing irregularity orthogonal to the firing rate in information representation. The scheme is valid if an interspike interval distribution can be well fitted by the gamma distribution and the firing irregularity is constant over time. We investigated in a computational model whether fluctuating external inputs may generate gamma process-like spike outputs, and whether the two quantities are actually decoupled. Whole-cell patch-clamp recordings of cortical neurons were performed to confirm the predictions of the model. The output spikes were well fitted by the gamma distribution. The firing irregularity remained approximately constant regardless of the firing rate when we injected a balanced input, in which excitatory and inhibitory synapses are activated concurrently while keeping their conductance ratio fixed. The degree of irregular firing depended on the effective reversal potential set by the balance between excitation and inhibition. In contrast, when we modulated conductances out of balance, the irregularity varied with the firing rate. These results indicate that the balanced input may improve the efficiency of neural coding by clamping the firing irregularity of cortical neurons. We demonstrate how this novel coding scheme facilitates stimulus decoding.

Power-Law Inter-Spike Interval Distributions Infer a Conditional Maximization of Entropy in Cortical Neurons

The brain is considered to use a relatively small amount of energy for its efficient information processing. Under a severe restriction on the energy consumption, the maximization of mutual information (MMI), which is adequate for designing artificial processing machines, may not suit for the brain. The MMI attempts to send information as accurate as possible and this usually requires a sufficient energy supply for establishing clearly discretized communication bands. Here, we derive an alternative hypothesis for neural code from the neuronal activities recorded juxtacellularly in the sensorimotor cortex of behaving rats. Our hypothesis states that in vivo cortical neurons maximize the entropy of neuronal firing under two constraints, one limiting the energy consumption (as assumed previously) and one restricting the uncertainty in output spike sequences at given firing rate. Thus, the conditional maximization of firing-rate entropy (CMFE) solves a tradeoff between the energy cost and noise in neuronal response. In short, the CMFE sends a rich variety of information through broader communication bands (i.e., widely distributed firing rates) at the cost of accuracy. We demonstrate that the CMFE is reflected in the long-tailed, typically power law, distributions of inter-spike intervals obtained for the majority of recorded neurons. In other words, the power-law tails are more consistent with the CMFE rather than the MMI. Thus, we propose the mathematical principle by which cortical neurons may represent information about synaptic input into their output spike trains.

Similarity in Neuronal Firing Regimes across Mammalian Species

The architectonic subdivisions of the brain are believed to be functional modules, each processing parts of global functions. Previously, we showed that neurons in different regions operate in different firing regimes in monkeys. It is possible that firing regimes reflect differences in underlying information processing, and consequently the firing regimes in homologous regions across animal species might be similar. We analyzed neuronal spike trains recorded from behaving mice, rats, cats, and monkeys. The firing regularity differed systematically, with differences across regions in one species being greater than the differences in similar areas across species. Neuronal firing was consistently most regular in motor areas, nearly random in visual and prefrontal/medial prefrontal cortical areas, and bursting in the hippocampus in all animals examined. This suggests that firing regularity (or irregularity) plays a key role in neural computation in each functional subdivision, depending on the types of information being carried. SIGNIFICANCE STATEMENT By analyzing neuronal spike trains recorded from mice, rats, cats, and monkeys, we found that different brain regions have intrinsically different firing regimes that are more similar in homologous areas across species than across areas in one species. Because different regions in the brain are specialized for different functions, the present finding suggests that the different activity regimes of neurons are important for supporting different functions, so that appropriate neuronal codes can be used for different modalities.

Neural dynamics and information representation in microcircuits of motor cortex

The brain has to analyze and respond to external events that can change rapidly from time to time, suggesting that information processing by the brain may be essentially dynamic rather than static. The dynamical features of neural computation are of significant importance in motor cortex that governs the process of movement generation and learning. In this paper, we discuss these features based primarily on our recent findings on neural dynamics and information coding in the microcircuit of rat motor cortex. In fact, cortical neurons show a variety of dynamical behavior from rhythmic activity in various frequency bands to highly irregular spike firing. Of particular interest are the similarity and dissimilarity of the neuronal response properties in different layers of motor cortex. By conducting electrophysiological recordings in slice preparation, we report the phase response curves (PRCs) of neurons in different cortical layers to demonstrate their layer-dependent synchronization properties. We then study how motor cortex recruits task-related neurons in different layers for voluntary arm movements by simultaneous juxtacellular and multiunit recordings from behaving rats. The results suggest an interesting difference in the spectrum of functional activity between the superficial and deep layers. Furthermore, the task-related activities recorded from various layers exhibited power law distributions of inter-spike intervals (ISIs), in contrast to a general belief that ISIs obey Poisson or Gamma distributions in cortical neurons. We present a theoretical argument that this power law of in vivo neurons may represent the maximization of the entropy of firing rate with limited energy consumption of spike generation. Though further studies are required to fully clarify the functional implications of this coding principle, it may shed new light on information representations by neurons and circuits in motor cortex.

2010 Special Issue: Bayesian estimation of phase response curves

Phase response curve (PRC) of an oscillatory neuron describes the response of the neuron to external perturbation. The PRC is useful to predict synchronized dynamics of neurons; hence, its measurement from experimental data attracts increasing interest in neural science. This paper introduces a Bayesian method for estimating PRCs from data, which allows for the correlation of errors in explanatory and response variables of the PRC. The method is implemented with a replica exchange Monte Carlo technique; this avoids local minima and enables efficient calculation of posterior averages. A test with artificial data generated by the noisy Morris-Lecar equation shows that the proposed method outperforms conventional regression that ignores errors in the explanatory variable. Experimental data from the pyramidal cells in the rat motor cortex is also analyzed with the method; a case is found where the result with the proposed method is considerably different from that obtained by conventional regression.

Long-Tailed Statistics of Corticocortical EPSPs: Origin and Computational Role of Noise in Cortical Circuits

Neurons in the brain exhibit highly irregular asynchronous firing even without sensory stimulation. Here, we study the recently proposed hypothesis that a highly non-homogeneous distribution, typically lognormal distribution, of cortico-cortical EPSP (excitatory postsynaptic potential) accounts for the low-rate spontaneous irregular activity observed in vivo. When amplitude distribution of EPSPs among excitatory neuron pairs obeys the lognormal distribution, networks of leaky integrate-and-fire model neurons robustly show ongoing firing state with low firing rate. Moreover, consistent with cortical neurobiology, the obtained activity had high irregularity, low synchronicity, and dynamically balanced excitation-inhibition population activity. We derive effective evolution equations for excitatory and inhibitory population activities from a recurrent network of the leaky integrate-and-fire neurons coupled with highly non-homogeneous connections. Based on the evolution equation, we perfume stability analysis of nontrivial solutions of the equation and reveal underling mechanisms and computational functions of the noise in cortical circuits.