Embedding stochastic dynamics of the environment in spontaneous activity by prediction-based plasticity

  1. Department of Bioengineering, Imperial College London, London, UK

Peer review process

Not revised: This Reviewed Preprint includes the authors’ original preprint (without revision), an eLife assessment, and public reviews.

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Editors

  • Reviewing Editor
    Julijana Gjorgjieva
    Technical University of Munich, Freising, Germany
  • Senior Editor
    Michael Frank
    Brown University, Providence, United States of America

Reviewer #1 (Public Review):

In the presented manuscript, the authors investigate how neural networks can learn to replay presented sequences of activity. Their focus lies on the stochastic replay according to learned transition probabilities. They show that based on error-based excitatory and balance-based inhibitory plasticity networks can self-organize towards this goal. Finally, they demonstrate that these learning rules can recover experimental observations from song-bird song learning experiments.

Overall, the study appears well-executed and coherent, and the presentation is very clear and helpful. However, it remains somewhat vague regarding the novelty. The authors could elaborate on the experimental and theoretical impact of the study, and also discuss how their results relate to those of Kappel et al, and others (e.g., Kappel et al (doi.org/10.1371/journal.pcbi.1003511)). Overall, the work could benefit if there was either (A) a formal analysis or derivation of the plasticity rules involved and a formal justification of the usefulness of the resulting (learned) neural dynamics; and/or (B) a clear connection of the employed plasticity rules to biological plasticity and clear testable experimental predictions. Thus, overall, this is a good work with some room for improvement.

Reviewer #2 (Public Review):

Summary:

This work proposes a synaptic plasticity rule that explains the generation of learned stochastic dynamics during spontaneous activity. The proposed plasticity rule assumes that excitatory synapses seek to minimize the difference between the internal predicted activity and stimulus-evoked activity, and inhibitory synapses try to maintain the E-I balance by matching the excitatory activity. By implementing this plasticity rule in a spiking recurrent neural network, the authors show that the state-transition statistics of spontaneous excitatory activity agree with that of the learned stimulus patterns, which are reflected in the learned excitatory synaptic weights. The authors further demonstrate that inhibitory connections contribute to well-defined state transitions matching the transition patterns evoked by the stimulus. Finally, they show that this mechanism can be expanded to more complex state-transition structures including songbird neural data.

Strengths:

This study makes an important contribution to computational neuroscience, by proposing a possible synaptic plasticity mechanism underlying spontaneous generations of learned stochastic state-switching dynamics that are experimentally observed in the visual cortex and hippocampus. This work is also very clearly presented and well-written, and the authors conducted comprehensive simulations testing multiple hypotheses. Overall, I believe this is a well-conducted study providing interesting and novel aspects of the capacity of recurrent spiking neural networks with local synaptic plasticity.

Weaknesses:

This study is very well-thought-out and theoretically valuable to the neuroscience community, and I think the main weaknesses are in regard to how much biological realism is taken into account. For example, the proposed model assumes that only synapses targeting excitatory neurons are plastic, and uses an equal number of excitatory and inhibitory neurons.

The model also assumes Markovian state dynamics while biological systems can depend more on history. This limitation, however, is acknowledged in the Discussion.
Finally, to simulate spontaneous activity, the authors use a constant input of 0.3 throughout the study. Different amplitudes of constant input may correspond to different internal states, so it will be more convincing if the authors test the model with varying amplitudes of constant inputs.

Reviewer #3 (Public Review):

Summary:

Asabuki and Clopath study stochastic sequence learning in recurrent networks of Poisson spiking neurons that obey Dale's law. Inspired by previous modeling studies, they introduce two distinct learning rules, to adapt excitatory-to-excitatory and inhibitory-to-excitatory synaptic connections. Through a series of computer experiments, the authors demonstrate that their networks can learn to generate stochastic sequential patterns, where states correspond to non-overlapping sets of neurons (cell assemblies) and the state-transition conditional probabilities are first-order Markov, i.e., the transition to a given next state only depends on the current state. Finally, the authors use their model to reproduce certain experimental songbird data involving highly-predictable and highly-uncertain transitions between song syllables.

Strengths:

This is an easy-to-follow, well-written paper, whose results are likely easy to reproduce. The experiments are clear and well-explained. The study of songbird experimental data is a good feature of this paper; finches are classical model animals for understanding sequence learning in the brain. I also liked the study of rapid task-switching, it's a good-to-know type of result that is not very common in sequence learning papers.

Weaknesses:

While the general subject of this paper is very interesting, I missed a clear main result. The paper focuses on a simple family of sequence learning problems that are well-understood, namely first-order Markov sequences and fully visible (no-hidden-neuron) networks, studied extensively in prior work, including with spiking neurons. Thus, because the main results can be roughly summarized as examples of success, it is not entirely clear what the main point of the authors is.

Going into more detail, the first major weakness I see in this paper is the heuristic choice of learning rules. The paper studies Poisson spiking neurons (I return to this point below), for which learning rules can be derived from a statistical objective, typically maximum likelihood. For fully-visible networks, these rules take a simple form, similar in many ways to the E-to-E rule introduced by the authors. This more principled route provides quite a lot of additional understanding on what is to be expected from the learning process. For instance, should maximum likelihood learning succeed, it is not surprising that the statistics of the training sequence distribution are reproduced. Moreover, given that the networks are fully visible, I think that the maximum likelihood objective is a convex function of the weights, which then gives hope that the learning rule does succeed. And so on. This sort of learning rule has been studied in a series of papers by David Barber and colleagues [refs. 1, 2 below], who applied them to essentially the same problem of reproducing sequence statistics in recurrent fully-visible nets. It seems to me that one key difference is that the authors consider separate E and I populations, and find the need to introduce a balancing I-to-E learning rule.

Because the rules here are heuristic, a number of questions come to mind. Why these rules and not others - especially, as the authors do not discuss in detail how they could be implemented through biophysical mechanisms? When does learning succeed or fail? What is the main point being conveyed, and what is the contribution on top of the work of e.g. Barber, Brea, et al. (2013), or Pfister et al. (2004)?

The use of a Poisson spiking neuron model is the second major weakness of the study. A chief challenge in much of the cited work is to generate stochastic transitions from recurrent networks of deterministic neurons. The task the authors set out to do is much easier with stochastic neurons; it is reasonable that the network succeeds in reproducing Markovian sequences, given an appropriate learning rule. I believe that the main point comes from mapping abstract Markov states to assemblies of neurons. If I am right, I missed more analyses on this point, for instance on the impact that varying cell assembly size would have on the findings reported by the authors.

Finally, it was not entirely clear to me what the main fundamental point in the HVC data section was. Can the findings be roughly explained as follows: if we map syllables to cell assemblies, for high-uncertainty syllable-to-syllable transitions, it becomes harder to predict future neural activity? In other words, is the main point that the HVC encodes syllables by cell assemblies?

(1) Learning in Spiking Neural Assemblies, David Barber, 2002. URL: https://proceedings.neurips.cc/paper/2002/file/619205da514e83f869515c782a328d3c-Paper.pdf

(2) Correlated sequence learning in a network of spiking neurons usingmaximum likelihood, David Barber, Felix Agakov, 2002. URL: http://web4.cs.ucl.ac.uk/staff/D.Barber/publications/barber-agakov-TR0149.pdf

  1. Howard Hughes Medical Institute
  2. Wellcome Trust
  3. Max-Planck-Gesellschaft
  4. Knut and Alice Wallenberg Foundation