Neural waves and computation in a neural net model II: Data-like structures and the dynamics of episodic memory.

The computational resources of a neuromorphic network model introduced earlier were investigated in the first paper of this series. It was argued that a form of ubiquitous spontaneous local convolution enabled logical gate-like neural motifs to form into hierarchical feed-forward structures of the Hubel-Wiesel type. Here we investigate concomitant data-like structures and their dynamic rôle in memory formation, retrieval, and replay. The mechanisms give rise to the need for general inhibitory sculpting, and the simulation of the replay of episodic memories, well known in humans and recently observed in rats. Other consequences include explanations of such findings as the directional flows of neural waves in memory formation and retrieval, visual anomalies and memory deficits in schizophrenia, and the operation of GABA agonist drugs in suppressing episodic memories. We put forward the hypothesis that all neural logical operations and feature extractions are of the convolutional hierarchical type described here and in the earlier paper, and exemplified by the Hubel-Wiesel model of the visual cortex, but that in more general cases the precise geometric layering might be obscured and so far undetected.

Network motifs in cellular neurophysiology.

Concepts from network science and graph theory, including the framework of network motifs, have been frequently applied in studying neuronal networks and other biological complex systems. Network-based approaches can also be used to study the functions of individual neurons, where cellular elements such as ion channels and membrane voltage are conceptualized as nodes within a network, and their interactions are denoted by edges. Network motifs in this context provide functional building blocks that help to illuminate the principles of cellular neurophysiology. In this review we build a case that network motifs operating within neurons provide tools for defining the functional architecture of single-neuron physiology and neuronal adaptations. We highlight the presence of such computational motifs in the cellular mechanisms underlying action potential generation, neuronal oscillations, dendritic integration, and neuronal plasticity. Future work applying the network motifs perspective may help to decipher the functional complexities of neurons and their adaptation during health and disease.

An operating principle of the cerebral cortex, and a cellular mechanism for attentional trial-and-error pattern learning and useful classification extraction.

A feature of the brains of intelligent animals is the ability to learn to respond to an ensemble of active neuronal inputs with a behaviorally appropriate ensemble of active neuronal outputs. Previously, a hypothesis was proposed on how this mechanism is implemented at the cellular level within the neocortical pyramidal neuron: the apical tuft or perisomatic inputs initiate "guess" neuron firings, while the basal dendrites identify input patterns based on excited synaptic clusters, with the cluster excitation strength adjusted based on reward feedback. This simple mechanism allows neurons to learn to classify their inputs in a surprisingly intelligent manner. Here, we revise and extend this hypothesis. We modify synaptic plasticity rules to align with behavioral time scale synaptic plasticity (BTSP) observed in hippocampal area CA1, making the framework more biophysically and behaviorally plausible. The neurons for the guess firings are selected in a voluntary manner via feedback connections to apical tufts in the neocortical layer 1, leading to dendritic Ca2+ spikes with burst firing, which are postulated to be neural correlates of attentional, aware processing. Once learned, the neuronal input classification is executed without voluntary or conscious control, enabling hierarchical incremental learning of classifications that is effective in our inherently classifiable world. In addition to voluntary, we propose that pyramidal neuron burst firing can be involuntary, also initiated via apical tuft inputs, drawing attention toward important cues such as novelty and noxious stimuli. We classify the excitations of neocortical pyramidal neurons into four categories based on their excitation pathway: attentional versus automatic and voluntary/acquired versus involuntary. Additionally, we hypothesize that dendrites within pyramidal neuron minicolumn bundles are coupled via depolarization cross-induction, enabling minicolumn functions such as the creation of powerful hierarchical "hyperneurons" and the internal representation of the external world. We suggest building blocks to extend the microcircuit theory to network-level processing, which, interestingly, yields variants resembling the artificial neural networks currently in use. On a more speculative note, we conjecture that principles of intelligence in universes governed by certain types of physical laws might resemble ours.

Neural waves and computation in a neural net model I: Convolutional hierarchies.

The computational resources of a neuromorphic network model introduced earlier are investigated in the context of such hierarchical systems as the mammalian visual cortex. It is argued that a form of ubiquitous spontaneous local convolution, driven by spontaneously arising wave-like activity-which itself promotes local Hebbian modulation-enables logical gate-like neural motifs to form into hierarchical feed-forward structures of the Hubel-Wiesel type. Extra-synaptic effects are shown to play a significant rôle in these processes. The type of logic that emerges is not Boolean, confirming and extending earlier findings on the logic of schizophrenia.

Neural heterogeneity controls computations in spiking neural networks.

The brain is composed of complex networks of interacting neurons that express considerable heterogeneity in their physiology and spiking characteristics. How does this neural heterogeneity influence macroscopic neural dynamics, and how might it contribute to neural computation? In this work, we use a mean-field model to investigate computation in heterogeneous neural networks, by studying how the heterogeneity of cell spiking thresholds affects three key computational functions of a neural population: the gating, encoding, and decoding of neural signals. Our results suggest that heterogeneity serves different computational functions in different cell types. In inhibitory interneurons, varying the degree of spike threshold heterogeneity allows them to gate the propagation of neural signals in a reciprocally coupled excitatory population. Whereas homogeneous interneurons impose synchronized dynamics that narrow the dynamic repertoire of the excitatory neurons, heterogeneous interneurons act as an inhibitory offset while preserving excitatory neuron function. Spike threshold heterogeneity also controls the entrainment properties of neural networks to periodic input, thus affecting the temporal gating of synaptic inputs. Among excitatory neurons, heterogeneity increases the dimensionality of neural dynamics, improving the network's capacity to perform decoding tasks. Conversely, homogeneous networks suffer in their capacity for function generation, but excel at encoding signals via multistable dynamic regimes. Drawing from these findings, we propose intra-cell-type heterogeneity as a mechanism for sculpting the computational properties of local circuits of excitatory and inhibitory spiking neurons, permitting the same canonical microcircuit to be tuned for diverse computational tasks.

Reproduced neuron-like excitability and bursting synchronization of memristive Josephson junctions loaded inductor.

Employing electronic component including memristor and Josephson junction to mimic biological neuron or synapse has elicited intense research in recent years. Neurons described by nonlinear oscillators can exhibit complex electrical activities. Josephson junctions are excellent candidates for neuron-inspired components because of their physical properties with low energy costs and high efficiency. In this paper, we revisit a prior work on memristive Josephson junction (MJJ) to identify the dynamical mechanisms to mimic neuron-like excitability and spiking. The inductive memristive Josephson junction (L-MJJ) model is further developed by adding an inductor with internal resistor. It is found that the L-MJJ model can reproduce square-wave bursting of the classical neuronal model from the neurodynamics point of view. The coupling L-MJJ oscillators can achieve in-phase and antiphase bursting synchronization similar with nonlinear coupling neurons. From the framework of nonlinear dynamics theory, this work aspires to build effective bridge between superconducting physics and theoretical neuroscience. Obtained results confirm the potential feasibility of this junction in designing a neuron-inspired computation to explore dynamics of larger-scale neuromorphic network.

A thermodynamical model of non-deterministic computation in cortical neural networks.

Neuronal populations in the cerebral cortex engage in probabilistic coding, effectively encoding the state of the surrounding environment with high accuracy and extraordinary energy efficiency. A new approach models the inherently probabilistic nature of cortical neuron signaling outcomes as a thermodynamic process of non-deterministic computation. A mean field approach is used, with the trial Hamiltonian maximizing available free energy and minimizing the net quantity of entropy, compared with a reference Hamiltonian. Thermodynamic quantities are always conserved during the computation; free energy must be expended to produce information, and free energy is released during information compression, as correlations are identified between the encoding system and its surrounding environment. Due to the relationship between the Gibbs free energy equation and the Nernst equation, any increase in free energy is paired with a local decrease in membrane potential. As a result, this process of thermodynamic computation adjusts the likelihood of each neuron firing an action potential. This model shows that non-deterministic signaling outcomes can be achieved by noisy cortical neurons, through an energy-efficient computational process that involves optimally redistributing a Hamiltonian over some time evolution. Calculations demonstrate that the energy efficiency of the human brain is consistent with this model of non-deterministic computation, with net entropy production far too low to retain the assumptions of a classical system.

Excitation creates a distributed pattern of cortical suppression due to varied recurrent input.

Dense local, recurrent connections are a major feature of cortical circuits, yet how they affect neurons' responses has been unclear, with some studies reporting weak recurrent effects, some reporting amplification, and others indicating local suppression. Here, we show that optogenetic input to mouse V1 excitatory neurons generates salt-and-pepper patterns of both excitation and suppression. Responses in individual neurons are not strongly predicted by that neuron's direct input. A balanced-state network model reconciles a set of diverse observations: the observed dynamics, suppressed responses, decoupling of input and output, and long tail of excited responses. The model shows recurrent excitatory-excitatory connections are strong and also variable across neurons. Together, these results demonstrate that excitatory recurrent connections can have major effects on cortical computations by shaping and changing neurons' responses to input.

A look into feedback neural computation upon collision selectivity.

Physiological studies have shown that a group of locust's lobula giant movement detectors (LGMDs) has a diversity of collision selectivity to approaching objects, relatively darker or brighter than their backgrounds in cluttered environments. Such diversity of collision selectivity can serve locusts to escape from attack by natural enemies, and migrate in swarm free of collision. For computational studies, endeavours have been made to realize the diverse selectivity which, however, is still one of the most challenging tasks especially in complex and dynamic real world scenarios. The existing models are mainly formulated as multi-layered neural networks with merely feed-forward information processing, and do not take into account the effect of re-entrant signals in feedback loop, which is an essential regulatory loop for motion perception, yet never been explored in looming perception. In this paper, we inaugurate feedback neural computation for constructing a new LGMD-based model, named F-LGMD to look into the efficacy upon implementing different collision selectivity. Accordingly, the proposed neural network model features both feed-forward processing and feedback loop. The feedback control propagates output signals of parallel ON/OFF channels back into their starting neurons, thus makes part of the feed-forward neural network, i.e. the ON/OFF channels and the feedback loop form an iterative cycle system. Moreover, the feedback control is instantaneous, which leads to the existence of a fixed point whereby the fixed point theorem is applied to rigorously derive valid range of feedback coefficients. To verify the effectiveness of the proposed method, we conduct systematic experiments covering synthetic and natural collision datasets, and also online robotic tests. The experimental results show that the F-LGMD, with a unified network, can fulfil the diverse collision selectivity revealed in physiology, which not only reduces considerably the handcrafted parameters compared to previous studies, but also offers a both efficient and robust scheme for collision perception through feedback neural computation.

How Flies See Motion.

How neurons detect the direction of motion is a prime example of neural computation: Motion vision is found in the visual systems of virtually all sighted animals, it is important for survival, and it requires interesting computations with well-defined linear and nonlinear processing steps-yet the whole process is of moderate complexity. The genetic methods available in the fruit fly Drosophila and the charting of a connectome of its visual system have led to rapid progress and unprecedented detail in our understanding of how neurons compute the direction of motion in this organism. The picture that emerged incorporates not only the identity, morphology, and synaptic connectivity of each neuron involved but also its neurotransmitters, its receptors, and their subcellular localization. Together with the neurons' membrane potential responses to visual stimulation, this information provides the basis for a biophysically realistic model of the circuit that computes the direction of visual motion.

A neural mechanism for terminating decisions.

The brain makes decisions by accumulating evidence until there is enough to stop and choose. Neural mechanisms of evidence accumulation are established in association cortex, but the site and mechanism of termination are unknown. Here, we show that the superior colliculus (SC) plays a causal role in terminating decisions, and we provide evidence for a mechanism by which this occurs. We recorded simultaneously from neurons in the lateral intraparietal area (LIP) and SC while monkeys made perceptual decisions. Despite similar trial-averaged activity, we found distinct single-trial dynamics in the two areas: LIP displayed drift-diffusion dynamics and SC displayed bursting dynamics. We hypothesized that the bursts manifest a threshold mechanism applied to signals represented in LIP to terminate the decision. Consistent with this hypothesis, SC inactivation produced behavioral effects diagnostic of an impaired threshold sensor and prolonged the buildup of activity in LIP. The results reveal the transformation from deliberation to commitment.

Object-centered population coding in CA1 of the hippocampus.

Objects and landmarks are crucial for guiding navigation and must be integrated into the cognitive map of space. Studies of object coding in the hippocampus have primarily focused on activity of single cells. Here, we record simultaneously from large numbers of hippocampal CA1 neurons to determine how the presence of a salient object in the environment alters single-neuron and neural-population activity of the area. The majority of the cells showed some change in their spatial firing patterns when the object was introduced. At the neural-population level, these changes were systematically organized according to the animal's distance from the object. This organization was widely distributed across the cell sample, suggesting that some features of cognitive maps-including object representation-are best understood as emergent properties of neural populations.

Amplified cortical neural responses as animals learn to use novel activity patterns.

Cerebral cortex supports representations of the world in patterns of neural activity, used by the brain to make decisions and guide behavior. Past work has found diverse, or limited, changes in the primary sensory cortex in response to learning, suggesting that the key computations might occur in downstream regions. Alternatively, sensory cortical changes may be central to learning. We studied cortical learning by using controlled inputs we insert: we trained mice to recognize entirely novel, non-sensory patterns of cortical activity in the primary visual cortex (V1) created by optogenetic stimulation. As animals learned to use these novel patterns, we found that their detection abilities improved by an order of magnitude or more. The behavioral change was accompanied by large increases in V1 neural responses to fixed optogenetic input. Neural response amplification to novel optogenetic inputs had little effect on existing visual sensory responses. A recurrent cortical model shows that this amplification can be achieved by a small mean shift in recurrent network synaptic strength. Amplification would seem to be desirable to improve decision-making in a detection task; therefore, these results suggest that adult recurrent cortical plasticity plays a significant role in improving behavioral performance during learning.

Consciousness, Exascale Computational Power, Probabilistic Outcomes, and Energetic Efficiency.

A central problem in the cognitive sciences is identifying the link between consciousness and neural computation. The key features of consciousness-including the emergence of representative information content and the initiation of volitional action-are correlated with neural activity in the cerebral cortex, but not computational processes in spinal reflex circuits or classical computing architecture. To take a new approach toward considering the problem of consciousness, it may be worth re-examining some outstanding puzzles in neuroscience, focusing on differences between the cerebral cortex and spinal reflex circuits. First, the mammalian cerebral cortex exhibits exascale computational power, a feature that is not strictly correlated with the number of binary computational units; second, individual computational units engage in noisy coding, allowing random electrical events to gate signaling outcomes; third, this noisy coding results in the synchronous firing of statistically random populations of cells across the neural network, at a range of nested frequencies; fourth, the system grows into a more ordered state over time, as it encodes the predictive value gained through observation; and finally, the cerebral cortex is extraordinarily energy efficient, with very little free energy lost to entropy during the work of information processing. Here, I argue that each of these five key features suggest the mammalian brain engages in probabilistic computation. Indeed, by modeling the physical mechanisms of probabilistic computation, we may find a better way to explain the unique emergent features arising from cortical neural networks.

The Computational and Neural Bases of Context-Dependent Learning.

Flexible behavior requires the creation, updating, and expression of memories to depend on context. While the neural underpinnings of each of these processes have been intensively studied, recent advances in computational modeling revealed a key challenge in context-dependent learning that had been largely ignored previously: Under naturalistic conditions, context is typically uncertain, necessitating contextual inference. We review a theoretical approach to formalizing context-dependent learning in the face of contextual uncertainty and the core computations it requires. We show how this approach begins to organize a large body of disparate experimental observations, from multiple levels of brain organization (including circuits, systems, and behavior) and multiple brain regions (most prominently the prefrontal cortex, the hippocampus, and motor cortices), into a coherent framework. We argue that contextual inference may also be key to understanding continual learning in the brain. This theory-driven perspective places contextual inference as a core component of learning.

Attention along the cortical hierarchy: Development matters.

We build on the existing biased competition view to argue that attention is an emergent property of neural computations within and across hierarchically embedded and structurally connected cortical pathways. Critically then, one must ask, what is attention emergent from? Within this framework, developmental changes in the quality of sensory input and feedforward-feedback information flow shape the emergence and efficiency of attention. Several gradients of developing structural and functional cortical architecture across the caudal-to-rostral axis provide the substrate for attention to emerge. Neural activity within visual areas depends on neuronal density, receptive field size, tuning properties of neurons, and the location of and competition between features and objects in the visual field. These visual cortical properties highlight the information processing bottleneck attention needs to resolve. Recurrent feedforward and feedback connections convey sensory information through a series of steps at each level of the cortical hierarchy, integrating sensory information across the entire extent of the cortical hierarchy and linking sensory processing to higher-order brain regions. Higher-order regions concurrently provide input conveying behavioral context and goals. Thus, attention reflects the output of a series of complex biased competition neural computations that occur within and across hierarchically embedded cortical regions. Cortical development proceeds along the caudal-to-rostral axis, mirroring the flow in sensory information from caudal to rostral regions, and visual processing continues to develop into childhood. Examining both typical and atypical development will offer critical mechanistic insight not otherwise available in the adult stable state. This article is categorized under: Psychology > Attention.

Systematic reduction of the dimensionality of natural scenes allows accurate predictions of retinal ganglion cell spike outputs.

The mammalian retina engages a broad array of linear and nonlinear circuit mechanisms to convert natural scenes into retinal ganglion cell (RGC) spike outputs. Although many individual integration mechanisms are well understood, we know less about how multiple mechanisms interact to encode the complex spatial features present in natural inputs. Here, we identified key spatial features in natural scenes that shape encoding by primate parasol RGCs. Our approach identified simplifications in the spatial structure of natural scenes that minimally altered RGC spike responses. We observed that reducing natural movies into 16 linearly integrated regions described ∼80% of the structure of parasol RGC spike responses; this performance depended on the number of regions but not their precise spatial locations. We used simplified stimuli to design high-dimensional metamers that recapitulated responses to naturalistic movies. Finally, we modeled the retinal computations that convert flashed natural images into one-dimensional spike counts.

Neuronal avalanche dynamics and functional connectivity elucidate information propagation in vitro.

Cascading activity is commonly observed in complex dynamical systems, including networks of biological neurons, and how these cascades spread through the system is reliant on how the elements of the system are connected and organized. In this work, we studied networks of neurons as they matured over 50 days in vitro and evaluated both their dynamics and their functional connectivity structures by observing their electrophysiological activity using microelectrode array recordings. Correlations were obtained between features of their activity propagation and functional connectivity characteristics to elucidate the interplay between dynamics and structure. The results indicate that in vitro networks maintain a slightly subcritical state by striking a balance between integration and segregation. Our work demonstrates the complementarity of these two approaches-functional connectivity and avalanche dynamics-in studying information propagation in neurons in vitro, which can in turn inform the design and optimization of engineered computational substrates.

Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection.

Neurons receive information through their synaptic inputs, but the functional significance of how those inputs are mapped on to a cell's dendrites remains unclear. We studied this question in a grasshopper visual neuron that tracks approaching objects and triggers escape behavior before an impending collision. In response to black approaching objects, the neuron receives OFF excitatory inputs that form a retinotopic map of the visual field onto compartmentalized, distal dendrites. Subsequent processing of these OFF inputs by active membrane conductances allows the neuron to discriminate the spatial coherence of such stimuli. In contrast, we show that ON excitatory synaptic inputs activated by white approaching objects map in a random manner onto a more proximal dendritic field of the same neuron. The lack of retinotopic synaptic arrangement results in the neuron's inability to discriminate the coherence of white approaching stimuli. Yet, the neuron retains the ability to discriminate stimulus coherence for checkered stimuli of mixed ON/OFF polarity. The coarser mapping and processing of ON stimuli thus has a minimal impact, while reducing the total energetic cost of the circuit. Further, we show that these differences in ON/OFF neuronal processing are behaviorally relevant, being tightly correlated with the animal's escape behavior to light and dark stimuli of variable coherence. Our results show that the synaptic mapping of excitatory inputs affects the fine stimulus discrimination ability of single neurons and document the resulting functional impact on behavior.

On the Tuning of the Computation Capability of Spiking Neural Membrane Systems with Communication on Request.

Spiking neural P systems (abbreviated as SNP systems) are models of computation that mimic the behavior of biological neurons. The spiking neural P systems with communication on request (abbreviated as SNQP systems) are a recently developed class of SNP system, where a neuron actively requests spikes from the neighboring neurons instead of passively receiving spikes. It is already known that small SNQP systems, with four unbounded neurons, can achieve Turing universality. In this context, 'unbounded' means that the number of spikes in a neuron is not capped. This work investigates the dependency of the number of unbounded neurons on the computation capability of SNQP systems. Specifically, we prove that (1) SNQP systems composed entirely of bounded neurons can characterize the family of finite sets of numbers; (2) SNQP systems containing two unbounded neurons are capable of generating the family of semilinear sets of numbers; (3) SNQP systems containing three unbounded neurons are capable of generating nonsemilinear sets of numbers. Moreover, it is obtained in a constructive way that SNQP systems with two unbounded neurons compute the operations of Boolean logic gates, i.e., OR, AND, NOT, and XOR gates. These theoretical findings demonstrate that the number of unbounded neurons is a key parameter that influences the computation capability of SNQP systems.