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Animals likely use a variety of strategies to solve laboratory tasks. Traditionally, combined analysis of behavioral and neural recording data across subjects employing different strategies may obscure important signals and give confusing results. Hence it is important to develop techniques that can infer strategy at the single-subject level. We analyzed an experiment in which two monkeys perform a visually cued rule-based task. From the analysis of their performance there is no indication that they used a different strategy. However, when we examined the geometry of stimulus representations in the state space of the neural activities recorded in dorsolateral prefrontal cortex, we found striking differences. Our purely neural results predict behavioral differences that we observed by analyzing the reaction times. These analyses provide strong support that the animals employed different strategies. Finally, we used a modeling study to correlate these strategies with the amount of training that the animals received.

Animals associate cues with outcomes and continually update these associations as new information is presented. The hippocampus is crucial for this, yet how neurons track changes in cue-outcome associations remains unclear. Using 2-photon calcium imaging, we tracked the same dCA1 and vCA1 neurons across days to determine how responses evolve across phases of odor-outcome learning. We find that, initially, odors elicited robust responses in dCA1, whereas in vCA1 responses emerged after learning, including broad representations that stretched across cue, trace, and outcome periods. Population dynamics in both regions rapidly reorganized with learning, then stabilized into ensembles that stored odor representations for days, even after extinction or pairing with a different outcome. Finally, we found stable, robust signals across CA1 when anticipating reward, but not when anticipating inescapable shock. These results identify how the hippocampus encodes, stores, and updates learned associations, and illuminates the unique contributions of dorsal and ventral hippocampus.

The firing rates of individual neurons displaying mixed selectivity are modulated by multiple task variables. When mixed selectivity is nonlinear, it confers an advantage by generating a high-dimensional neural representation that can be flexibly decoded by linear classifiers. Although the advantages of this coding scheme are well accepted, the means of designing an experiment and analyzing the data to test for and characterize mixed selectivity remain unclear. With the growing number of large datasets collected during complex tasks, the mixed selectivity is increasingly observed and is challenging to interpret correctly. We review recent approaches for analyzing and interpreting neural datasets and clarify the theoretical implications of mixed selectivity in the variety of forms that have been reported in the literature. We also aim to provide a practical guide for determining whether a neural population has linear or nonlinear mixed selectivity and whether this mixing leads to a categorical or category-free representation.

SUMMARYAnimals associate cues with outcomes and continually update these associations as new information is presented. The hippocampus is crucial for this, yet how neurons track changes in cue-outcome associations remains unclear. Using 2-photon calcium imaging, we tracked the same dCA1 and vCA1 neurons across days to determine how responses evolve across phases of odor-outcome learning. We find that, initially, odors elicited robust responses in dCA1, whereas in vCA1 responses emerged after learning, including broad representations that stretched across cue, trace, and outcome periods. Population dynamics in both regions rapidly reorganized with learning, then stabilized into ensembles that stored odor representations for days, even after extinction or pairing with a different outcome. Finally, we found stable, robust signals across CA1 when anticipating reward, but not when anticipating inescapable shock. These results identify how the hippocampus encodes, stores, and updates learned associations, and illuminates the unique contributions of dorsal and ventral hippocampus.

Neurons are often considered as specialized functional units that encode a single variable. However, many neurons are observed to respond to a mix of disparate sensory, cognitive and behavioral variables. For such representations information is distributed across multiple neurons. Here we find this distributed code in the dentate gyrus and CA1 subregions of the hippocampus. Using calcium imaging in freely moving mice, we decoded the animal’s position, direction of motion and speed from the activity of hundreds of cells. The response properties of individual neurons were only partially predictive of their importance for encoding position. Non-place cells encoded position and contributed to position encoding when combined together with other cells. Indeed, disrupting the correlations between neural activities decreased decoding performance, mostly in CA1. Our analysis indicates that population methods, rather than classical analyses based on single cell response properties, may more accurately characterize the neural code in the hippocampus.

Animals must discern important stimuli and place them onto their cognitive map of their environment. The neocortex conveys general representations of sensory events to the hippocampus, and the hippocampus is thought to classify and sharpen the distinctions between these events. We recorded populations of dentate gyrus granule cells (DG GCs) and lateral entorhinal cortex (LEC) neurons across days to understand how sensory representations are modified by experience. We found representations of odors in DG GCs that required synaptic input from the LEC. Odor classification accuracy in DG GCs correlated with future behavioral discrimination. In associative learning, DG GCs, more so than LEC neurons, changed their responses to odor stimuli, increasing the distance in neural representations between stimuli, responding more to the conditioned and less to the unconditioned odorant. Thus, with learning, DG GCs amplify the decodability of cortical representations of important stimuli, which may facilitate information storage to guide behavior.

Episodic memory requires linking events in time, a function dependent on the hippocampus. In “trace” fear conditioning, animals learn to associate a neutral cue with an aversive stimulus despite their separation in time by a delay period on the order of tens of seconds. But how this temporal association forms remains unclear. Here we use 2-photon calcium imaging to track neural population dynamics over the complete time-course of learning and show that, in contrast to previous theories, the hippocampus does not generate persistent activity to bridge the time delay. Instead, learning is concomitant with broad changes in the active neural population in CA1. While neural responses were highly stochastic in time, cue identity could be reliably read out from population activity rates over longer timescales after learning. These results question the ubiquity of neural sequences during temporal association learning, and suggest that trace fear conditioning relies on mechanisms that differ from persistent activity accounts of working memory.

Episodic memory requires linking events in time, a function dependent on the hippocampus. In "trace" fear conditioning, animals learn to associate a neutral cue with an aversive stimulus despite their separation in time by a delay period on the order of tens of seconds. But how this temporal association forms remains unclear. Here we use two-photon calcium imaging of neural population dynamics throughout the course of learning and show that, in contrast to previous theories, hippocampal CA1 does not generate persistent activity to bridge the delay. Instead, learning is concomitant with broad changes in the active neural population. Although neural responses were stochastic in time, cue identity could be read out from population activity over longer timescales after learning. These results question the ubiquity of seconds-long neural sequences during temporal association learning and suggest that trace fear conditioning relies on mechanisms that differ from persistent activity accounts of working memory.

The tuning properties of neurons in a given brain region have been traditionally viewed as the under-pinnings of computation in neural circuits. However, at the higher levels of processing, specialization is often elusive, instead a mix of sensory, cognitive and behavioural quantities drive neural activity. In such networks, ensembles of neurons, rather than single units with easily interpretable tuning properties, encode behaviourally relevant variables. Here we show that this is the case also in the dentate gyrus and CA1 subregions of the hippocampus. Using calcium imaging in freely moving mice, we decoded the instantaneous position, direction of motion and speed from the activity of hundreds of cells in the hippocampus of mice freely exploring an arena. For the vast majority of neurons in both regions, their response properties were not predictive of their importance for encoding position. Furthermore, we could decode position from populations of cells that were important for decoding direction of motion and vice versa, showing that these quantities are encoded by largely overlapping ensembles as in distributed neural code. Finally, we found that correlated activities had an impact on decoding performance in CA1 but not in dentate gyrus, suggesting different enconding strategies for these areas. Our analysis indicates that classical methods of analysis based on single cell response properties might be insufficient to accurately characterize the neural computation in a given area. In contrast, population analysis may help highlight previously overlooked properties of hippocampal circuits.

The statistical characterization of the spatial structure of large animal groups has been very limited so far, mainly due to a lack of empirical data, especially in three dimensions (3D). Here we focus on the case of large flocks of starlings (Sturnus vulgaris) in the field. We reconstruct the 3D positions of individual birds within flocks of up to few thousands of elements. In this respect our data constitute a unique set. We perform a statistical analysis of flocks' structure by using two quantities that are new to the field of collective animal behaviour, namely the conditional density and the pair correlation function. These tools were originally developed in the context of condensed matter theory. We explain what is the meaning of these two quantities, how to measure them in a reliable way, and why they are useful in assessing the density fluctuations and the statistical correlations across the group. We show that the border-to-centre density gradient displayed by starling flocks gives rise to an anomalous behaviour of the conditional density. We also find that the pair correlation function has a structure incompatible with a crystalline arrangement of birds. In fact, our results suggest that flocks are somewhat intermediate between the liquid and the gas phase of physical systems. (C) 2008 Elsevier Inc. All rights reserved.

Implementing compact, low-power artificial neural processing systems with real-time on-line learning abilities is still an open challenge. In this paper we present a full-custom mixed-signal VLSI device with neuromorphic learning circuits that emulate the biophysics of real spiking neurons and dynamic synapses for exploring the properties of computational neuroscience models and for building brain-inspired computing systems. The proposed architecture allows the on-chip configuration of a wide range of network connectivities, including recurrent and deep networks, with short-term and long-term plasticity. The device comprises 128 K analog synapse and 256 neuron circuits with biologically plausible dynamics and bi-stable spike-based plasticity mechanisms that endow it with on-line learning abilities. In addition to the analog circuits, the device comprises also asynchronous digital logic circuits for setting different synapse and neuron properties as well as different network configurations. This prototype device, fabricated using a 180 nm 1P6M CMOS process, occupies an area of 51.4 mm2, and consumes approximately 4 mW for typical experiments, for example involving attractor networks. Here we describe the details of the overall architecture and of the individual circuits and present experimental results that showcase its potential. By supporting a wide range of cortical-like computational modules comprising plasticity mechanisms, this device will enable the realization of intelligent autonomous systems with on-line learning capabilities., Frontiers in Neuroscience, 9, ISSN:1662-453X, ISSN:1662-4548

Extending bidirectional brain-machine interfaces (BMI) tailored for specific experiments with additional software and hardware tools can be very onerous, if not impossible. To overcome this problem, we developed a modular configurable system by modifying the architecture of an existing bidirectional BMI. This modular system enables the seamless and efficient inclusion of new features and the integration of new protocols without changing the native system's overall structure. By introducing a platform for the implementation of BMI algorithms on neuromorphic chips, this method represents a step towards the development of low-power, compact and computationally powerful tools for clinical applications.

Neuromorphic hardware offers an electronic substrate for the realization of asynchronous event-based sensory-motor systems and large-scale spiking neural network architectures. In order to characterize these systems, configure them, and carry out modeling experiments, it is often necessary to interface them to workstations. The software used for this purpose typically consists of a large monolithic block of code which is highly specific to the hardware setup used. While this approach can lead to highly integrated hardware/software systems, it hampers the development of modular and reconfigurable infrastructures thus preventing a rapid evolution of such systems. To alleviate this problem, we propose PyNCS, an open-source front-end for the definition of neural network models that is interfaced to the hardware through a set of Python Application Programming Interfaces (APIs). The design of PyNCS promotes modularity, portability and expandability and separates implementation from hardware description. The high-level front-end that comes with PyNCS includes tools to define neural network models as well as to create, monitor and analyze spiking data. Here we report the design philosophy behind the PyNCS framework and describe its implementation. We demonstrate its functionality with two representative case studies, one using an event-based neuromorphic vision sensor, and one using a set of multi-neuron devices for carrying out a cognitive decision-making task involving state-dependent computation. PyNCS, already applicable to a wide range of existing spike-based neuromorphic setups, will accelerate the development of hybrid software/hardware neuromorphic systems, thanks to its code flexibility. The code is open-source and available online at https://github.com/inincs/pyNCS., Frontiers in Neuroinformatics, 8, ISSN:1662-5196

To endow large scale VLSI networks of spiking neurons with learning abilities it is important to develop compact and low power circuits that implement synaptic plasticity mechanisms. In this paper we present an analog/digital Spike-Timing Dependent Plasticity (STDP) circuit that changes its internal state in a continuous analog way on short biologically plausible time scales and drives its weight to one of two possible bi-stable states on long time scales. We highlight the differences and improvements over previously proposed circuits and demonstrate the performance of the new circuit using data measured from a chip fabricated using a standard 180nm CMOS process. Finally we discuss the use of stochastic learning methods that can best exploit the properties of this circuit for implementing robust machine-learning algorithms.

Several analog and digital brain-inspired electronic systems have been recently proposed as dedicated solutions for fast simulations of spiking neural networks. While these architectures are useful for exploring the computational properties of large-scale models of the nervous system, the challenge of building low-power compact physical artifacts that can behave intelligently in the real-world and exhibit cognitive abilities still remains open. In this paper we propose a set of neuromorphic engineering solutions to address this challenge. In particular, we review neuromorphic circuits for emulating neural and synaptic dynamics in real-time and discuss the role of biophysically realistic temporal dynamics in hardware neural processing architectures; we review the challenges of realizing spike-based plasticity mechanisms in real physical systems and present examples of analog electronic circuits that implement them; we describe the computational properties of recurrent neural networks and show how neuromorphic Winner-Take-All circuits can implement working-memory and decision-making mechanisms. We validate the neuromorphic approach proposed with experimental results obtained from our own circuits and systems, and argue how the circuits and networks presented in this work represent a useful set of components for efficiently and elegantly implementing neuromorphic cognition., Comment: Submitted to Proceedings of IEEE, spiking neural network implementations in full custom VLSI

From bird flocks to fish schools, animal groups often seem to react to environmental perturbations as if of one mind. Most studies in collective animal behavior have aimed to understand how a globally ordered state may emerge from simple behavioral rules. Less effort has been devoted to understanding the origin of collective response, namely the way the group as a whole reacts to its environment. Yet, in the presence of strong predatory pressure on the group, collective response may yield a significant adaptive advantage. Here we suggest that collective response in animal groups may be achieved through scale-free behavioral correlations. By reconstructing the 3D position and velocity of individual birds in large flocks of starlings, we measured to what extent the velocity fluctuations of different birds are correlated to each other. We found that the range of such spatial correlation does not have a constant value, but it scales with the linear size of the flock. This result indicates that behavioral correlations are scale free: The change in the behavioral state of one animal affects and is affected by that of all other animals in the group, no matter how large the group is. Scale-free correlations provide each animal with an effective perception range much larger than the direct interindividual interaction range, thus enhancing global response to perturbations. Our results suggest that flocks behave as critical systems, poised to respond maximally to environmental perturbations.

I fenomeni di comportamento collettivo animale da secoli affascinano scienziati e filosofi. Una delle moderne sfide della fisica e quella di spiegare i fenomeni di organizzazione spontanea osservati in natura, come quello della formazione di stormi, attraverso l’uso di tecniche proprie della meccanica statistica. In questo lavoro e stato necessario progettare e realizzare un apparato sperimentale innovativo per la ricostruzione tridimensionale delle singole posizioni e delle traiettorie di singoli storni in volo durante le loro note evoluzioni aeree. Per la prima volta e stato possibile ottenere dei risultati numerici che riguardano sia quantita statiche (densita, forma, distribuzione, ecc.) che quantita dinamiche (correlazioni di velocita, lunghezza diffusione, relazioni di vicinanza, ecc.) in stormi di storni composti da un numero variabile di individui dalle decine alle migliaia.

Animal groups represent magnificent archetypes of self-organized collective behavior. As such, they have attracted enormous interdisciplinary interest in the last years. From a mechanistic point of view, animal aggregations remind physical systems of particles or spins, where the individual constituents interact locally, giving rise to ordering at the global scale. This analogy has fostered important research, where numerical and theoretical approaches from physics have been applied to models of self-organized motion. In this paper, we discuss how the physics methodology may provide precious conceptual and technical instruments in empirical studies of collective animal behavior. We focus on three-dimensional groups, for which empirical data have been extremely scarce until recently, and describe novel experimental protocols that allow reconstructing aggregations of thousands of individuals. We show how an appropriate statistical analysis of these large-scale data allows inferring important information on the interactions between individuals in a group, a key issue in behavioral studies and a basic ingredient of theoretical models. To this aim, we revisit the approach we recently used on starling flocks, and apply it to a much larger data set, never analyzed before. The results confirm our previous findings and indicate that interactions between birds have a topological rather than metric nature, each individual interacting with a fixed number of neighbors irrespective of their distances.

Spike-based learning circuits have been typically used in conjunction with linear integrate-and-flre neurons. As a new class of current-mode conductance-based silicon neurons has been recently developed, it is important to evaluate how the spike-based learning circuits perform, when interfaced to these new types of neuron circuits. Here, we describe a VLSI implementation of a current-mode conductance-based neuron, connected to synaptic circuits with spike-based learning capabilities. The conductance-based silicon neuron has built-in spike-frequency adaptation, refractory period mechanisms, and plasticity eligibility control circuits. The synaptic circuits exhibits realistic dynamics in the post-synaptic currents and comprise local spike-based learning circuits, controlled by the global post-synaptic eligibility circuits. We present experimental results which characterize the conductance-based neuron circuit properties and the spike-based learning circuits connected to it.

Olfactory stimuli are represented in a high- dimensional space by neural networks of the olfactory system. A great deal of research in olfaction has focused on this representation within the first processing stage, the olfactory bulb (vertebrates) or antennal lobe (insects) glomeruli. In particular the mapping of chemical stimuli onto olfactory glomeruli and the relation of this mapping to perceptual qualities have been investigated. While a number of studies have illustrated the importance of inhibitory networks within the olfactory bulb or the antennal lobe for the shaping and processing of olfactory information, it is not clear how exactly these inhibitory networks are organized to provide filtering and contrast enhancement capabilities. In this work the aim is to study the topology of the proposed networks by using software simulations and hardware implementation. While we can study the dependence of the activity on each parameter of the theoretical models with the simulations, it is important to understand whether the models can be used in robotic applications for real-time odor recognition. We present the results of a linear simulation, a spiking simulation with I&F neurons and a real-time hardware emulation using neuromorphic VLSI chips. We used an input data set of neurophysiological recordings from olfactory receptive neurons of insects, especially Drosophila.