A Non-spiking Neuron Model With Dynamic Leak to Avoid Instability in Recurrent Networks.

Recurrent circuitry components are distributed widely within the brain, including both excitatory and inhibitory synaptic connections. Recurrent neuronal networks have potential stability problems, perhaps a predisposition to epilepsy. More generally, instability risks making internal representations of information unreliable. To assess the inherent stability properties of such recurrent networks, we tested a linear summation, non-spiking neuron model with and without a "dynamic leak", corresponding to the low-pass filtering of synaptic input current by the RC circuit of the biological membrane. We first show that the output of this neuron model, in either of its two forms, follows its input at a higher fidelity than a wide range of spiking neuron models across a range of input frequencies. Then we constructed fully connected recurrent networks with equal numbers of excitatory and inhibitory neurons and randomly distributed weights across all synapses. When the networks were driven by pseudorandom sensory inputs with varying frequency, the recurrent network activity tended to induce high frequency self-amplifying components, sometimes evident as distinct transients, which were not present in the input data. The addition of a dynamic leak based on known membrane properties consistently removed such spurious high frequency noise across all networks. Furthermore, we found that the neuron model with dynamic leak imparts a network stability that seamlessly scales with the size of the network, conduction delays, the input density of the sensory signal and a wide range of synaptic weight distributions. Our findings suggest that neuronal dynamic leak serves the beneficial function of protecting recurrent neuronal circuitry from the self-induction of spurious high frequency signals, thereby permitting the brain to utilize this architectural circuitry component regardless of network size or recurrency.

Cuneate spiking neural network learning to classify naturalistic texture stimuli under varying sensing conditions.

We implemented a functional neuronal network that was able to learn and discriminate haptic features from biomimetic tactile sensor inputs using a two-layer spiking neuron model and homeostatic synaptic learning mechanism. The first order neuron model was used to emulate biological tactile afferents and the second order neuron model was used to emulate biological cuneate neurons. We have evaluated 10 naturalistic textures using a passive touch protocol, under varying sensing conditions. Tactile sensor data acquired with five textures under five sensing conditions were used for a synaptic learning process, to tune the synaptic weights between tactile afferents and cuneate neurons. Using post-learning synaptic weights, we evaluated the individual and population cuneate neuron responses by decoding across 10 stimuli, under varying sensing conditions. This resulted in a high decoding performance. We further validated the decoding performance across stimuli, irrespective of sensing velocities using a set of 25 cuneate neuron responses. This resulted in a median decoding performance of 96% across the set of cuneate neurons. Being able to learn and perform generalized discrimination across tactile stimuli, makes this functional spiking tactile system effective and suitable for further robotic applications.

Intracellular Dynamics in Cuneate Nucleus Neurons Support Self-Stabilizing Learning of Generalizable Tactile Representations.

How the brain represents the external world is an unresolved issue for neuroscience, which could provide fundamental insights into brain circuitry operation and solutions for artificial intelligence and robotics. The neurons of the cuneate nucleus form the first interface for the sense of touch in the brain. They were previously shown to have a highly skewed synaptic weight distribution for tactile primary afferent inputs, suggesting that their connectivity is strongly shaped by learning. Here we first characterized the intracellular dynamics and inhibitory synaptic inputs of cuneate neurons in vivo and modeled their integration of tactile sensory inputs. We then replaced the tactile inputs with input from a sensorized bionic fingertip and modeled the learning-induced representations that emerged from varied sensory experiences. The model reproduced both the intrinsic membrane dynamics and the synaptic weight distributions observed in cuneate neurons in vivo. In terms of higher level model properties, individual cuneate neurons learnt to identify specific sets of correlated sensors, which at the population level resulted in a decomposition of the sensor space into its recurring high-dimensional components. Such vector components could be applied to identify both past and novel sensory experiences and likely correspond to the fundamental haptic input features these neurons encode in vivo. In addition, we show that the cuneate learning architecture is robust to a wide range of intrinsic parameter settings due to the neuronal intrinsic dynamics. Therefore, the architecture is a potentially generic solution for forming versatile representations of the external world in different sensor systems.