Synaptic plasticity in medial vestibular nucleus neurons: comparison with computational requirements of VOR adaptation

Background: Vestibulo-ocular reflex (VOR) gain adaptation, a longstanding experimental model of cerebellar learning, utilizes sites of plasticity in both cerebellar cortex and brainstem. However, the mechanisms by which the activity of cortical Purkinje cells may guide synaptic plasticity in brainstem vestibular neurons are unclear. Theoretical analyses indicate that vestibular plasticity should depend upon the correlation between Purkinje cell and vestibular afferent inputs, so that, in gain-down learning for example, increased cortical activity should induce long-term depression (LTD) at vestibular synapses. Methodology/Principal Findings: Here we expressed this correlational learning rule in its simplest form, as an anti-Hebbian, heterosynaptic spike-timing dependent plasticity interaction between excitatory (vestibular) and inhibitory (floccular) inputs converging on medial vestibular nucleus (MVN) neurons (input-spike-timing dependent plasticity, iSTDP). To test this rule, we stimulated vestibular afferents to evoke EPSCs in rat MVN neurons in vitro. Control EPSC recordings were followed by an induction protocol where membrane hyperpolarizing pulses, mimicking IPSPs evoked by flocculus inputs, were paired with single vestibular nerve stimuli. A robust LTD developed at vestibular synapses when the afferent EPSPs coincided with membrane hyperpolarisation, while EPSPs occurring before or after the simulated IPSPs induced no lasting change. Furthermore, the iSTDP rule also successfully predicted the effects of a complex protocol using EPSP trains designed to mimic classical conditioning. Conclusions: These results, in strong support of theoretical predictions, suggest that the cerebellum alters the strength of vestibular synapses on MVN neurons through hetero-synaptic, anti-Hebbian iSTDP. Since the iSTDP rule does not depend on post-synaptic firing, it suggests a possible mechanism for VOR adaptation without compromising gaze-holding and VOR performance in vivo

Seven properties of self-organization in the human brain

The principle of self-organization has acquired a fundamental significance in the newly emerging field of computational philosophy. Self-organizing systems have been described in various domains in science and philosophy including physics, neuroscience, biology and medicine, ecology, and sociology. While system architecture and their general purpose may depend on domain-specific concepts and definitions, there are (at least) seven key properties of self-organization clearly identified in brain systems: 1) modular connectivity, 2) unsupervised learning, 3) adaptive ability, 4) functional resiliency, 5) functional plasticity, 6) from-local-to-global functional organization, and 7) dynamic system growth. These are defined here in the light of insight from neurobiology, cognitive neuroscience and Adaptive Resonance Theory (ART), and physics to show that self-organization achieves stability and functional plasticity while minimizing structural system complexity. A specific example informed by empirical research is discussed to illustrate how modularity, adaptive learning, and dynamic network growth enable stable yet plastic somatosensory representation for human grip force control. Implications for the design of “strong” artificial intelligence in robotics are brought forward

The effects of noise on binocular rivalry waves: a stochastic neural field model

We analyse the effects of extrinsic noise on traveling waves of visual perception in a competitive neural field model of binocular rivalry. The model consists of two one-dimensional excitatory neural fields, whose activity variables represent the responses to left-eye and right-eye stimuli, respectively. The two networks mutually inhibit each other, and slow adaptation is incorporated into the model by taking the network connections to exhibit synaptic depression. We first show how, in the absence of any noise, the system supports a propagating composite wave consisting of an invading activity front in one network co-moving with a retreating front in the other network. Using a separation of time scales and perturbation methods previously developed for stochastic reaction-diffusion equations, we then show how multiplicative noise in the activity variables leads to a diffusive–like displacement (wandering) of the composite wave from its uniformly translating position at long time scales, and fluctuations in the wave profile around its instantaneous position at short time scales. The multiplicative noise also renormalizes the mean speed of the wave. We use our analysis to calculate the first passage time distribution for a stochastic rivalry wave to travel a fixed distance, which we find to be given by an inverse Gaussian. Finally, we investigate the effects of noise in the depression variables, which under an adiabatic approximation leads to quenched disorder in the neural fields during propagation of a wave

Sleep-like slow oscillations improve visual classification through synaptic homeostasis and memory association in a thalamo-cortical model

The occurrence of sleep passed through the evolutionary sieve and is widespread in animal species. Sleep is known to be beneficial to cognitive and mnemonic tasks, while chronic sleep deprivation is detrimental. Despite the importance of the phenomenon, a complete understanding of its functions and underlying mechanisms is still lacking. In this paper, we show interesting effects of deep-sleep-like slow oscillation activity on a simplified thalamo-cortical model which is trained to encode, retrieve and classify images of handwritten digits. During slow oscillations, spike-timing-dependent-plasticity (STDP) produces a differential homeostatic process. It is characterized by both a specific unsupervised enhancement of connections among groups of neurons associated to instances of the same class (digit) and a simultaneous down-regulation of stronger synapses created by the training. This hierarchical organization of post-sleep internal representations favours higher performances in retrieval and classification tasks. The mechanism is based on the interaction between top-down cortico-thalamic predictions and bottom-up thalamo-cortical projections during deep-sleep-like slow oscillations. Indeed, when learned patterns are replayed during sleep, cortico-thalamo-cortical connections favour the activation of other neurons coding for similar thalamic inputs, promoting their association. Such mechanism hints at possible applications to artificial learning systems.Comment: 11 pages, 5 figures, v5 is the final version published on Scientific Reports journa

Top-down inputs enhance orientation selectivity in neurons of the primary visual cortex during perceptual learning.

Perceptual learning has been used to probe the mechanisms of cortical plasticity in the adult brain. Feedback projections are ubiquitous in the cortex, but little is known about their role in cortical plasticity. Here we explore the hypothesis that learning visual orientation discrimination involves learning-dependent plasticity of top-down feedback inputs from higher cortical areas, serving a different function from plasticity due to changes in recurrent connections within a cortical area. In a Hodgkin-Huxley-based spiking neural network model of visual cortex, we show that modulation of feedback inputs to V1 from higher cortical areas results in shunting inhibition in V1 neurons, which changes the response properties of V1 neurons. The orientation selectivity of V1 neurons is enhanced without changing orientation preference, preserving the topographic organizations in V1. These results provide new insights to the mechanisms of plasticity in the adult brain, reconciling apparently inconsistent experiments and providing a new hypothesis for a functional role of the feedback connections

Redistribution of Synaptic Efficacy Supports Stable Pattern Learning in Neural Networks

Markram and Tsodyks, by showing that the elevated synaptic efficacy observed with single-pulse LTP measurements disappears with higher-frequency test pulses, have critically challenged the conventional assumption that LTP reflects a general gain increase. Redistribution of synaptic efficacy (RSE) is here seen as the local realization of a global design principle in a neural network for pattern coding. As is typical of many coding systems, the network learns by dynamically balancing a pattern-independent increase in strength against a pattern-specific increase in selectivity. This computation is implemented by a monotonic long-term memory process which has a bidirectional effect on the postsynaptic potential via functionally complementary signal components. These frequency-dependent and frequency-independent components realize the balance between specific and nonspecific functions at each synapse. This synaptic balance suggests a functional purpose for RSE which, by dynamically bounding total memory change, implements a distributed coding scheme which is stable with fast as well as slow learning. Although RSE would seem to make it impossible to code high-frequency input features, a network preprocessing step called complement coding symmetrizes the input representation, which allows the system to encode high-frequency as well as low-frequency features in an input pattern. A possible physical model interprets the two synaptic signal components in terms of ligand-gated and voltage-gated receptors, where learning converts channels from one type to another.Office of Naval Research and the Defense Advanced Research Projects Agency (N00014-95-1-0409, N00014-1-95-0657