Learning by the Dendritic Prediction of Somatic Spiking
Open accessAbstract
Recent modeling of spike-timing-dependent plasticity indicates that plasticity involves as a third factor a local dendritic potential, besides pre- and postsynaptic firing times. We present a simple compartmental neuron model together with a non-Hebbian, biologically plausible learning rule for dendritic synapses where plasticity is modulated by these three factors. In functional terms, the rule seeks to minimize discrepancies between somatic firings and a local dendritic potential. Such prediction errors can arise in our model from stochastic fluctuations as well as from synaptic input, which directly targets the soma. Depending on the nature of this direct input, our plasticity rule subserves supervised or unsupervised learning. When a reward signal modulates the learning rate, reinforcement learning results. Hence a single plasticity rule supports diverse learning paradigms.
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One way to biologically implement the hippocampal replay as a target or 'teaching signal' for the FF neurons is to 'nudge' these neurons in the soma, while the synapses projecting from the FF pathway to their dendrites learn to reproduce the somatic nudging.
“One way to biologically implement the hippocampal replay as a target or 'teaching signal' for the FF neurons is to 'nudge' these neurons in the soma, while the synapses projecting from the FF pathway to their dendrites learn to reproduce the somatic nudging [59].”
From How Adversarial REM Dreams May Facilitate Creativity, and Why We Become Aware of Them (2024) · cites this paper as [59]
Such sub-networks might even be part of the same neuron and map onto apical vs. basal parts of the dendritic tree.
“Interestingly, such sub-networks might even be part of the same neuron and map onto “apical” vs. “basal” parts of the dendritic tree (Körding and König, 2001; Urbanczik and Senn, 2014).”
From Toward an integration of deep learning and neuroscience (2016) · cites this paper as Urbanczik and Senn, 2014
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Electrical Compartmentalization in Neurons
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Nair, M. V., Müller, L. K., & Indiveri, G. (2017) · Nano Futures · doi:10.1088/2399-1984/aa954a · Cited by 38 · see citing works
Brivio, S., Ly, D. R. B., Vianello, E., & Spiga, S. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.580909 · Cited by 37 · see citing works
“Among the spike-based training procedures, supervised learning rules inspired by the back-propagation exist (Urbanczik and Senn, 2014; Müller et al., 2017; Donati et al., 2019), which are seldom investigated for systems including realistic simulations of memristive devices (Nair et al., 2017;…”
Does computational neuroscience need new synaptic learning paradigms?
Brea, J., & Gerstner, W. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.05.012 · Cited by 38 · see citing works
Somatodendritic consistency check for temporal feature segmentation
Asabuki, T., & Fukai, T. (2020) · Nature Communications · doi:10.1038/s41467-020-15367-w · Cited by 36 · see citing works
Perceptron Learning and Classification in a Modeled Cortical Pyramidal Cell
Moldwin, T., & Segev, I. (2020) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2020.00033 · Cited by 35 · see citing works
“…treat clustering of nearby synapses, and “structural plasticity,” or the relocation of synaptic inputs within and between branches as crucial for learning (Trachtenberg et al., 2002; Larkum and Nevian, 2008; Losonczy et al., 2008; Kastellakis et al., 2015; Weber et al., 2016; Mel et al., 2017).”
BackgroundData-driven reduction of dendritic morphologies with preserved dendro-somatic responses
Wybo, W. A. M., Jordan, J., Ellenberger, B., Mengual, U. M., Nevian, T., & Senn, W. (2021) · eLife · doi:10.7554/elife.60936 · Cited by 35 · see citing works
“Finally, we change the average voltage level achieved by the combined AMPA and GABA input by changing the ‘nudging potential’ en (Urbanczik and Senn, 2014)”
MethodSelf-citationDendritic error backpropagation in deep cortical microcircuitsPreprint
Sacramento, J., Costa, R. P., Bengio, Y., & Senn, W. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1801.00062 · Cited by 52 · see citing works
“ough weights WPI k,k (see Fig. 1A). Additionally, cross-area feedback onto SST cells originating at the next higher brain area k+1 provide a weak nudging signal for these interneurons, modelled after Urbanczik and Senn (2014) as a conductance-based so4 matic input current. For computational simplicity, we modelled thi…”
InfluentialSelf-citationNeural and Synaptic Array Transceiver: A Brain-Inspired Computing Framework for Embedded Learning
Detorakis, G., Sheik, S., Augustine, C., Paul, S., Pedroni, B. U., Dutt, N. D., Krichmar, J. L., Cauwenberghs, G., & Neftci, E. O. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00583 · Cited by 33 · see citing works
“On the other hand, three factor rules solve this problem by adding a factor indicative of reward, error, gradients provided extrinsically or through other neural states (Clopath et al., 2010; Urbanczik and Senn, 2014).”
BackgroundMethodInfluentialSpike-driven threshold-based learning with memristive synapses and neuromorphic silicon neurons
Covi, E., George, R., Frascaroli, J., Brivio, S., Mayr, C., Mostafa, H., Indiveri, G., & Spiga, S. (2018) · Journal of Physics D Applied Physics · doi:10.1088/1361-6463/aad361 · Cited by 33 · see citing works
“New learning schemes involving spike rate [32, 33] and new plasticity models taking the rate of the synaptic activity into account [34 – 36] have therefore been proposed.”
BackgroundQuantum superposition inspired spiking neural network
Sun, Y., Zeng, Y., & Zhang, T. (2021) · iScience · doi:10.1016/j.isci.2021.102880 · Cited by 35 · see citing works
“Parameter Θ controls the proportion of original image and reverse image in background color inverse images with Learning procedure of the QS-SNN algorithm Dendrite prediction (Urbanczik and Senn, 2014) and proximal gradient methods are used for tuning of QS-SNN.”
BackgroundMethodContinual Learning in a Multi-Layer Network of an Electric Fish
Muller, S. Z., Zadina, A. N., Abbott, L. F., & Sawtell, N. B. (2019) · Cell · doi:10.1016/j.cell.2019.10.020 · Cited by 33 · see citing works
“Related twocompartment neuronal models have been proposed on theoretical grounds as biologically plausible implementations of machine-learning schemes in cerebral cortical circuits (Guerguiev et al., 2017; Kording and Konig, 2001; Marblestone et al., 2016; Schiess et al., 2016; Urbanczik and Senn, 2014).”
BackgroundPredictive Processing: A Circuit Approach to Psychosis
Keller, G. B., & Sterzer, P. (2024) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100223-121214 · Cited by 47 · see citing works
Attractor network dynamics enable preplay and rapid path planning in maze-like environments
Corneil, D., & Gerstner, W. (2015) · Infoscience (Ecole Polytechnique Fédérale de Lausanne) · Cited by 31 · see citing works
Evolving interpretable plasticity for spiking networks
Jordan, J., Schmidt, M., Senn, W., & Petrovici, M. A. (2021) · eLife · doi:10.7554/elife.66273 · Cited by 30 · see citing works
“For the purpose of this study, we implemented a reward-driven (Urbanczik and Senn, 2009) and an errordriven learning rule (Equation 7; Urbanczik and Senn, 2014), as well as a homeostatic STDP rule (Equation 17; Masquelier, 2018) via custom C++ code.”
Self-citationLearning cortical representations through perturbed and adversarial dreaming
Deperrois, N., Petrovici, M. A., Senn, W., & Jordan, J. (2022) · eLife · doi:10.7554/elife.76384 · Cited by 28 · see citing works
“…in cortical networks through different classes of pyramidal neurons with a biological version of supervised learning based on a dendritic prediction of somatic activity (Urbanczik and Senn, 2014), and a corresponding global modulation of synaptic plasticity by state-specific neuromodulators.”
BackgroundMethodSelf-citationCapone, C., Lupo, C., Muratore, P., & Paolucci, P. S. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2220743120 · Cited by 27 · see citing works
Learning accurate path integration in ring attractor models of the head direction system
Vafidis, P., Owald, D., D’Albis, T., & Kempter, R. (2022) · eLife · doi:10.7554/elife.69841 · Cited by 25 · see citing works
Omission responses in local field potentials in rat auditory cortex
Auksztulewicz, R., Rajendran, V. G., Peng, F., Schnupp, J. W. H., & Harper, N. S. (2023) · BMC Biology · doi:10.1186/s12915-023-01592-4 · Cited by 26 · see citing works
Functional architecture of intracellular oscillations in hippocampal dendrites
Liao, Z., Gonzalez, K. C., Li, D. M., Yang, C. M., Holder, D. J., McClain, N. E., Zhang, G., Evans, S. W., Chavarha, M., Simko, J., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50546-z · Cited by 30 · see citing works
Remme, M. W. H., Bergmann, U., Alevi, D., Schreiber, S., Sprekeler, H., & Kempter, R. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009681 · Cited by 27 · see citing works
“This can be achieved by STDP in combination with longer transmission delays in the indirect pathway, as suggested here, but other neural implementations of supervised learning may be equally suitable [42, 43, 70].”
BackgroundOn-chip Few-shot Learning with Surrogate Gradient Descent on a Neuromorphic Processor
Stewart, K. M., Orchard, G., Shrestha, S. B., & Neftci, E. O. (2020) · IEEE International Conference on Artificial Intelligence Circuits and Systems (AICAS) · doi:10.1109/aicas48895.2020.9073948 · Cited by 24 · see citing works
“Such rules are compatible with a wide number of unsupervised, supervised, and reinforcement learning paradigms [11], and implementations can have scaling properties comparable to that of STDP [12].”
BackgroundMercier, M. S., Magloire, V., Cornford, J. H., & Kullmann, D. M. (2022) · The Journal of Physiology · doi:10.1113/jp282753 · Cited by 22 · see citing works
“Payeur et al., 2021; Richards & Lillicrap, 2019; Sacramento et al., 2018; Urbanczik & Senn, 2014).”
Structural plasticity on an accelerated analog neuromorphic hardware system
Billaudelle, S., Cramer, B., Petrovici, M. A., Schreiber, K., Kappel, D., Schemmel, J., & Meier, K. (2020) · Neural Networks · doi:10.1016/j.neunet.2020.09.024 · Cited by 24 · see citing works
Frenkel, C., Bol, D., & Indiveri, G. (2021) · Zurich Open Repository and Archive (University of Zurich) · doi:10.5167/uzh-217499 · Cited by 24 · see citing works
Learning cortical representations through perturbed and adversarial dreaming.
Deperrois, N., Petrovici, M. A., Senn, W., & Jordan, J. (2022) · doi:10.48350/169088 · Cited by 24 · see citing works
Self-citationCredit Assignment in Neural Networks through Deep Feedback Control
Meulemans, A., Farinha, M. T., Ordóñez, J. G., Aceituno, P. V., Sacramento, J., & Grewe, B. F. (2021) · Repository for Publications and Research Data (ETH Zurich) · doi:10.3929/ethz-b-000529286 · Cited by 22 · see citing works
A neuronal least-action principle for real-time learning in cortical circuits
Senn, W., Dold, D., Kungl, Á. F., Ellenberger, B., Jordan, J., Bengio, Y., Sacramento, J., & Petrovici, M. A. (2024) · eLife · doi:10.1101/2023.03.25.534198 · Cited by 22 · see citing works
“Each network neuron performs gradient descent on its own dendritic prediction error (Urbanczik & Senn, 2014), and with this eventually also contributes to a reduction of the output errors.”
InfluentialSelf-citationBhasin, B. J., Raymond, J. L., & Goldman, M. S. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2406010121 · Cited by 21 · see citing works
Learning of Precise Spike Times with Homeostatic Membrane Potential Dependent Synaptic Plasticity
Albers, C., Westkott, M., & Pawelzik, K. R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148948 · Cited by 21 · see citing works
“Also, it is worth noting that the model of Urbanczik and Senn requires a one-way barrier to prevent somatic voltage invading the dendrites; in contrast, MPDP requires a strong two-way coupling between somatic and dendritic/synaptic voltage.”
BackgroundInfluentialOn the relationship between predictive coding and backpropagation
Rosenbaum, R. (2022) · PLoS ONE · doi:10.1371/journal.pone.0266102 · Cited by 20 · see citing works
“Backpropagation can be performed using local updates if gradients of neurons’ activations are passed upstream through feedback connections, but this interpretation implies other biologically implausible properties of the”
BackgroundDendrites and efficiency: Optimizing performance and resource utilization
Makarov, R., Pagkalos, M., & Poirazi, P. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102812 · Cited by 23 · see citing works
“A mismatch between the apical prediction signal and somatic spiking results in top-down prediction error [47].”
Sun, Y., Zhao, F., Zhao, Z., & Zeng, Y. (2024) · Neural Networks · doi:10.1016/j.neunet.2024.106898 · Cited by 20 · see citing works
“…employ multi-compartment neuron (MCN) models for tasks involving simple stimulus classification and image recognition, such as MNIST images (Urbanczik and Senn, 2014; Sacramento, Ponte Costa, Bengio and Senn, 2018) and neuron spiking sequences (Zhang, Yang, Ma, Wu, Li and Tan, 2024; Li,…”
Noise Gated by Dendrosomatic Interactions Increases Information Transmission
Naud, R., Payeur, A., & Longtin, A. (2017) · Physical Review X · doi:10.1103/physrevx.7.031045 · Cited by 18 · see citing works
Frenkel, C., Lefebvre, M., & Bol, D. (2019) · Cited by 17 · see citing works
Geng, H.-Y., Arbuthnott, G. W., Yung, W., & Ke, Y. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab460 · Cited by 26 · see citing works
Gao, T. Y., Deng, B., Wang, J., & Yi, G. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.929644 · Cited by 16 · see citing works
“Urbanczik and Senn (2014) minimize the discrepancies between somatic firings and local dendritic potential to train their SNN.”
BackgroundSpecific connectivity optimizes learning in thalamocortical loops
Lakshminarasimhan, K. J., Xie, M., Cohen, J. D., Sauerbrei, B., Hantman, A. W., Litwin-Kumar, A., & Escola, G. S. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114059 · Cited by 17 · see citing works
“…in the cortex might undergo more sophisticated forms of plasticity by leveraging the complex dendritic machinery involving distinct apical and basal compartments, 49,70 such structures are absent in the thalamus and therefore cannot be used to perform credit assignment in corticothalamic synapses.”
BackgroundLearning efficient backprojections across cortical hierarchies in real time
Max, K., Kriener, L., García, G. P., Nowotny, T., Jaras, I., Senn, W., & Petrovici, M. A. (2024) · Nature Machine Intelligence · doi:10.1038/s42256-024-00845-3 · Cited by 16 · see citing works
“In this model, weights are adapted using local dendritic plasticity rules in the form ̇ W = η [ φ ( u ) − φ ( v )] r T , where W represents lateral or feed-forwards weights, η is a learning rate, u and v denote different compartmental voltages and r the presynaptic rate 63,64 .”
Self-citationLearning to represent signals spike by spike
Brendel, W., Bourdoukan, R., Vertechi, P., Machens, C. K., & Denève, S. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007692 · Cited by 20 · see citing works
“In the future, these ideas may be combined with explicit single-neuron models [53] to turn local learning rules into global functions [21,52,54].”
Embodied Synaptic Plasticity With Online Reinforcement Learning
Kaiser, J., Hoff, M., Konle, A., Tieck, J. C. V., Kappel, D., Reichard, D., Subramoney, A., Legenstein, R. A., Roennau, A., Maass, W., et al. (2019) · Frontiers in Neurorobotics · doi:10.3389/fnbot.2019.00081 · Cited by 14 · see citing works
“2 Closed-Loop Embodiment Implementation Usually, synaptic learning rules are solely evaluated on open-loop pattern classification tasks [46, 32, 35, 41].”
BackgroundInfluentialNeural circuit mechanisms of hierarchical sequence learning tested on large-scale recording data
Asabuki, T., Kokate, P., & Fukai, T. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010214 · Cited by 15 · see citing works
A Biologically Plausible Neural Network for Multichannel Canonical Correlation Analysis
Lipshutz, D., Bahroun, Y., Golkar, S., Sengupta, A. M., & Chklovskii, D. B. (2021) · Neural Computation · doi:10.1162/neco_a_01414 · Cited by 15 · see citing works
“Multi-compartmental models of pyramidal neurons have been invoked previously in the context of biological implementation of the backpropagation algorithm [26, 48, 21, 22, 44, 43].”
BackgroundMethodParallel and Recurrent Cascade Models as a Unifying Force for Understanding Subcellular Computation
Harkin, E. F., Shen, P. R., Goel, A., Richards, B. A., & Naud, R. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.07.026 · Cited by 15 · see citing works
Feedforward Initialization for Fast Inference of Deep Generative Networks is biologically plausiblePreprint
Bengio, Y., Scellier, B., Bilaniuk, O., Sacramento, J., & Senn, W. (2016) · arXiv (Cornell University) · doi:10.48550/arxiv.1606.01651 · Cited by 15 · see citing works
“23 can also be seen in the context of dendritic predictions of somatic spiking (Urbanczik and Senn, 2014).”
BackgroundMethodInfluentialSelf-citationAlternating Excitation–Inhibition Dendritic Computing for Classification
Li, J., Lei, Z., Zhang, Z., Li, H., Todo, Y., & Gao, S. (2024) · IEEE Transactions on Artificial Intelligence · doi:10.1109/tai.2024.3416236 · Cited by 14 · see citing works
Moldwin, T., Kalmenson, M., & Segev, I. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009015 · Cited by 14 · see citing works
Predictive coding with spiking neurons and feedforward gist signaling
Lee, K., Dora, S., Mejias, J. F., Bohte, S. M., & Pennartz, C. M. A. (2024) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2024.1338280 · Cited by 14 · see citing works
- Authors
- Urbanczik, R., & Senn, W.
- Affiliations
- University of Bern (CH)
- Corresponding author
- Senn, Walter
- ORCID
- Senn, Walter
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 81
- Issue
- 3
- Pages
- 521-528
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2006814548
- Cited by
- 230
- References
- 31
- Citations by year
- 2026: 14 · 2025: 19 · 2024: 44 · 2023: 19 · 2022: 23 · 2021: 30 · 2020: 29 · 2019: 11 · 2018: 12 · 2017: 13 · 2016: 11 · 2015: 3 · 2014: 2
- FWCI
- 5.38
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Physical Sciences › Engineering › Electrical and Electronic Engineering › Advanced Memory and Neural Computing
- Keywords
- spike-timing-dependent plasticity, dendritic potentials, compartmental neuron model, dendritic synapses, prediction error, stochastic fluctuations, supervised learning, unsupervised learning, reinforcement learning
- MeSH terms
- Action Potentials, Animals, Computer Simulation, Dendrites, Learning, Models, Neurological, Neuronal Plasticity, Neurons, Synapses, Time Factors
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