Biology subjects

Priesemann, V.

Publications and source records attributed to Priesemann, V..

12 recordsLinked to original sources

bioRxiv2025

Continuous dynamics of cooperation and competition in social foraging

Real-life social interactions often unfold continuously and involve dynamic cooperation and competition, yet most studies rely on discrete games that do not capture the adaptive and graded nature of continuous sensorimotor decisions. To address this gap, we developed the Cooperation-Competition Foraging game -- an ecologically grounded paradigm in which pairs of participants (dyads) navigate a continuous shared space under face-to-face visibility, deciding in real-time to collect rewarded targets either individually or jointly. Dyads (n=58, 116 participants) spontaneously converged on distinct stable strategies along the cooperation-competition spectrum, forming three groups: cooperative, intermediate, and competitive. Despite the behavioral complexity, our computational model, which incorporated travel path minimization, sensorimotor communication, and recent choice history, predicted dyadic decisions with 87% accuracy, and linked prediction certainty with ensuing dynamics of spatiotemporal coordination. Further modeling revealed how sensorimotor factors, such as movement speed and skill, shape distinct strategies and payoffs. Crucially, we quantify the cost of cooperation, demonstrating that in many dyads prosocial tendencies outweigh the individual benefits of exploiting skill advantages. Our versatile framework provides a predictive, mechanistic account of how social and embodied drivers promote the emergence of dynamic cooperation and competition, and offers rigorous metrics for investigating the neural basis of naturalistic social interactions, and for linking personality traits to distinct strategies.

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bioRxiv2024

Inferring Effective Networks of Spiking Neurons Using a Continuous-Time Estimator of Transfer Entropy

When analysing high-dimensional time-series datasets, the inference of effective networks has proven to be a valuable modelling technique. This technique produces networks where each target node is associated with a set of source nodes that are capable of providing explanatory power for its dynamics. Multivariate Transfer Entropy (TE) has proven to be a popular and effective tool for inferring these networks. Recently, a continuous-time estimator of TE for event-based data such as spike trains has been developed which, in more efficiently representing event data in terms of inter-event intervals, is significantly more capable of measuring multivariate interactions. The new estimator thus presents an opportunity to more effectively use TE for the inference of effective networks from spike trains, and we demonstrate in this paper for the first time its efficacy at this task. Using data generated from models of spiking neurons -- for which the ground-truth connectivity is known -- we demonstrate the accuracy of this approach in various dynamical regimes. We further show that it exhibits far superior inference performance to a pairwise TE-based approach as well as a recently-proposed convolutional neural network approach. Moreover, comparison with Generalised Linear Models (GLMs), which are commonly applied to spike-train data, showed clear benefits, particularly in cases of high synchrony. Finally, we demonstrate its utility in revealing the patterns by which effective connections develop from recordings of developing neural cell cultures.

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bioRxiv2024

Power-law adaptation in the presynaptic vesicle cycle

After synaptic transmission, fused synaptic vesicles are recycled, enabling the synapse to recover its capacity for renewed release. The recovery steps, which range from endocytosis to vesicle docking and priming, have been studied individually, but it is not clear what their impact on the overall dynamics of synaptic recycling is, and how they influence signal transmission. Here we model the dynamics of vesicle recycling and find that the multiple timescales of the recycling steps are reflected in synaptic recovery. This leads to multi-timescale synapse dynamics, which can be described by a simplified synaptic model with power-law adaptation. Using cultured hippocampal neurons, we test this model experimentally, and show that the duration of synaptic exhaustion changes the effective synaptic recovery timescale, as predicted by the model. Finally, we show that this adaptation could implement a specific function in the hippocampus, namely enabling efficient communication between neurons through the temporal whitening of hippocampal spike trains.

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bioRxiv2023

Prediction mismatch responses arise as corrections of a predictive spiking code

Prediction mismatch responses in cortex seem to signal the difference between an internal model of the animal and sensory observations. Often these responses are interpreted as evidence for the existence of error neurons, which guide inference in models of hierarchical predictive coding. Here we show that prediction mismatch responses also arise naturally in a spiking encoding of sensory signals, where spikes predict the future signal. In this model, the predictive representation has to be corrected when a mispredicted stimulus appears, which requires additional neural activity. This adaptive correction could explain why mismatch response latency can vary with mismatch detection difficulty, as the network gathers sensory evidence before committing to a correction. Prediction mismatch responses thus might not reflect the computation of errors per se, but rather the reorganization of the neural code when new information is incorporated.

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bioRxiv2022

Visuomotor mismatch responses as a hallmark of explaining away in causal inference

How are visuomotor mismatch responses in visual cortex embedded into cortical processing? We here argue that mismatch responses are best understood as the result of a cooperation of motor and visual areas to jointly explain optic flow. This cooperation ensures that optic flow is not explained redundantly by both areas, which in the language of causal inference is termed explaining away. This improves the efficiency of the resulting neural code, and allows the animal to easily detect movements that are independent of its own locomotion. We demonstrate the emergence of mismatch responses from explaining away in simulations, where spiking neurons learn to encode optic flow stimuli and locomotion. We furthermore lay out arguments against the prevailing idea that mismatch signals are the result of a dedicated error computation in a hierarchical model. These results provide a new perspective on several recent experiments of cross-modal neural interactions in cortex.

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bioRxiv2021

Perception and propagation of activity through the cortical hierarchy is determined by neural variability

The brains of higher organisms are composed of anatomically and functionally distinct regions performing specialised tasks; but regions do not operate in isolation. Orchestration of complex behaviours requires communication between brain regions, but how neural activity dynamics are organised to facilitate reliable transmission is not well understood. We studied this process directly by generating neural activity that propagates between brain regions and drives behaviour, allowing us to assess how populations of neurons in sensory cortex cooperate to transmit information. We achieved this by imaging two hierarchically organised and densely interconnected regions, the primary and secondary somatosensory cortex (S1 and S2) in mice while performing two-photon photostimulation of S1 neurons and assigning behavioural salience to the photostimulation. We found that the probability of perception is determined not only by the strength of the photostimulation signal, but also by the variability of S1 neural activity. Therefore, maximising the signal-to-noise ratio of the stimulus representation in cortex relative to the noise or variability in cortex is critical to facilitate activity propagation and perception. Further, we show that propagated, behaviourally salient activity elicits balanced, persistent, and generalised activation of the downstream region. Hence, our work adds to existing understanding of cortical function by identifying how population activity is formatted to ensure robust transmission of information, allowing specialised brain regions to communicate and coordinate behaviour.

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bioRxiv2021

Early lock-in of structured and specialised information flows during neural development

The brains of many organisms are capable of complicated distributed computation underpinned by a highly advanced information processing capacity. Although substantial progress has been made towards characterising the information flow component of this capacity in mature brains, there is a distinct lack of work characterising its emergence during neural development. This lack of progress has been largely driven by the lack of effective estimators of information processing operations for the spiking data available for developing neural networks. Here, we leverage recent advances in this estimation task in order to quantify the changes in information flow during development. We do so by studying the changes in the intrinsic dynamics of the spontaneous activity of developing dissociated neural cell cultures. We find that the quantity of information flowing across these networks undergoes a dramatic increase across development. Moreover, the spatial structure of these flows is locked-in during early development, after which there is a substantial temporal correlation in the information flows across recording days. We analyse the flow of information during the crucial periods of population bursts. We find that, during these bursts, nodes undertake specialised computational roles as either transmitters, mediators or receivers of information, with these roles tending to align with their spike ordering -- either early, mid or late in the bursts. Further, we find that the specialised computational roles occupied by nodes during bursts tend to be locked-in early. Finally, we briefly compare these results to information flows in a model network developing according to an STDP learning rule from a state of independent firing to synchronous bursting. The phenomena of large increases in information flow, early lock-in of information flow spatial structure and computational roles based on burst position were also observed in this model, hinting at the broader generality of these phenomena. AUTHOR SUMMARYThis paper studies the development of computation in biological systems by analysing changes in the flow of information in developing neural cell cultures. Although there have been a number of previous studies of information flows in neural cell cultures, this work represents the first study which compares information flows in the intrinsic dynamics across development time. Moreover, we make use of a recently proposed continuous-time transfer entropy estimator for spike trains, which, in comparison to the discrete-time estimator used previously, is able to capture important effects occurring on both small and large timescales simultaneously. We find that information flows begin to emerge after 5-10 days of activity, and crucially, the spatial structure of information flows remains significantly temporally correlated over the first month of recording. Furthermore, the magnitude of information flows across the culture are strongly related to burst position, and the roles of regions as information flow sources, sinks and mediators are found to remain consistent across development. Finally, we confirm that these early lock-ins also occur in a simple model network developing under an STDP update rule, suggesting a plausible mechanism undergirding this phenomenon.

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bioRxiv2020

Embedding optimization reveals long-lasting history dependence in neural spiking activity

Information processing can leave distinct footprints on the statistics of neural spiking. For example, efficient coding minimizes the statistical dependencies on the spiking history, while temporal integration of information may require the maintenance of information over different timescales. To investigate these footprints, we developed a novel approach to quantify history dependence within the spiking of a single neuron, using the mutual information between the entire past and current spiking. This measure captures how much past information is necessary to predict current spiking. In contrast, classical time-lagged measures of temporal dependence like the autocorrelation capture how long--potentially redundant--past information can still be read out. Strikingly, we find for model neurons that our method disentangles the strength and timescale of history dependence, whereas the two are mixed in classical approaches. When applying the method to experimental data, which are necessarily of limited size, a reliable estimation of mutual information is only possible for a coarse temporal binning of past spiking, a so called past embedding. To still account for the vastly different spiking statistics and potentially long history dependence of living neurons, we developed an embedding-optimization approach that does not only vary the number and size, but also an exponential stretching of past bins. For extra-cellular spike recordings, we found that the strength and timescale of history dependence indeed can vary independently across experimental preparations. While hippocampus indicated strong and long history dependence, in visual cortex it was weak and short, while in vitro the history dependence was strong but short. This work enables an information theoretic characterization of history dependence in recorded spike trains, which captures a footprint of information processing that is beyond time-lagged measures of temporal dependence. To facilitate the application of the method, we provide practical guidelines and a toolbox. Author summaryEven with exciting advances in recording techniques of neural spiking activity, experiments only provide a comparably short glimpse into the activity of only a tiny subset of all neurons. How can we learn from these experiments about the organization of information processing in the brain? To that end, we exploit that different properties of information processing leave distinct footprints on the firing statistics of individual spiking neurons. In our work, we focus on a particular statistical footprint: How much does a single neurons spiking depend on its own preceding activity, which we call history dependence. By quantifying history dependence in neural spike recordings, one can, in turn, infer some of the properties of information processing. Because recording lengths are limited in practice, a direct estimation of history dependence from experiments is challenging. The embedding optimization approach that we present in this paper aims at extracting a maximum of history dependence within the limits set by a reliable estimation. The approach is highly adaptive and thereby enables a meaningful comparison of history dependence between neurons with vastly different spiking statistics, which we exemplify on a diversity of spike recordings. In conjunction with recent, highly parallel spike recording techniques, the approach could yield valuable insights on how hierarchical processing is organized in the brain.

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bioRxiv2020

Sequence memory in recurrent neuronal network can develop without structured input

How does spontaneous activity during development prepare cortico-cortical connections for sensory input? We here analyse the development of sequence memory, an intrinsic feature of recurrent networks that supports temporal perception. We use a recurrent neural network model with homeostatic and spike-timing-dependent plasticity (STDP). This model has been shown to learn specific sequences from structured input. We show that development even under unstructured input increases unspecific sequence memory. Moreover, networks "pre-shaped" by such unstructured input subsequently learn specific sequences faster. The key structural substrate is the emergence of strong and directed synapses due to STDP and synaptic competition. These construct self-amplifying preferential paths of activity, which can quickly encode new input sequences. Our results suggest that memory traces are not printed on a tabula rasa, but instead harness building blocks already present in the brain.

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bioRxiv2019

A unified picture of neuronal avalanches arises from the understanding of sampling effects

To date, it is still impossible to sample the entire mammalian brain with single-neuron precision. This forces one to either use spikes (focusing on few neurons) or to use coarse-sampled activity (averaging over many neurons, e.g. LFP). Naturally, the sampling technique impacts inference about collective properties. Here, we emulate both sampling techniques on a spiking model to quantify how they alter observed correlations and signatures of criticality. We discover a general effect: when the inter-electrode distance is small, electrodes sample overlapping regions in space, which increases the correlation between the signals. For coarse-sampled activity, this can produce power-law distributions even for non-critical systems. In contrast, spike recordings enable one to distinguish the underlying dynamics. This explains why coarse measures and spikes have produced contradicting results in the past - that are now all consistent with a slightly subcritical regime.

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bioRxiv2018

Inference, validation and predictions about statistics and propagation of cortical spiking in vivo

Electrophysiological recordings of spiking activity can only access a small fraction of all neurons simultaneously. This spatial subsampling has hindered characterizing even most basic properties of collective spiking in cortex. In particular, two contradictory hypotheses prevailed for over a decade: the first proposed an asynchronous irregular, the second a critical state. While distinguishing them is straightforward in models, we show that in experiments classical approaches fail to infer them correctly, because subsampling can bias measures as basic as the correlation strength. Deploying a novel, subsampling-invariant estimator, we find evidence that in vivo cortical dynamics clearly differs from asynchronous or critical dynamics, and instead occupies a narrow \"reverberating\" regime, consistently across multiple mammalian species and cortical areas. These results enabled us to predict cortical properties that are difficult or impossible to obtain experimentally, including responses to minimal perturbations, intrinsic network timescales, and the strength of external input compared to recurrent activation.

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bioRxiv2018

Homeostatic plasticity and external input shape neural network dynamics

In vitro and in vivo spiking activity clearly differ. Whereas networks in vitro develop strong bursts separated by periods of very little spiking activity, in vivo cortical networks show continuous activity. This is puzzling considering that both networks presumably share similar single-neuron dynamics and plasticity rules. We propose that the defining difference between in vitro and in vivo dynamics is the strength of external input. In vitro, networks are virtually isolated, whereas in vivo every brain area receives continuous input. We analyze a model of spiking neurons in which the input strength, mediated by spike rate homeostasis, determines the characteristics of the dynamical state. In more detail, our analytical and numerical results on various network topologies show consistently that under increasing input, homeostatic plasticity generates distinct dynamic states, from bursting, to close-to-critical, reverberating and irregular states. This implies that the dynamic state of a neural network is not fixed but can readily adapt to the input strengths. Indeed, our results match experimental spike recordings in vitro and in vivo: the in vitro bursting behavior is consistent with a state generated by very low network input (< 0.1%), whereas in vivo activity suggests that on the order of 1% recorded spikes are input-driven, resulting in reverberating dynamics. Importantly, this predicts that one can abolish the ubiquitous bursts of in vitro preparations, and instead impose dynamics comparable to in vivo activity by exposing the system to weak long-term stimulation, thereby opening new paths to establish an in vivo-like assay in vitro for basic as well as neurological studies.

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