## Abstract

A vast majority of computation in the brain is performed by spiking neural networks. Despite the ubiquity of such spiking, we currently lack an understanding of how biological spiking neural circuits learn and compute in vivo, as well as how we can instantiate such capabilities in artificial spiking circuits in silico. Here we revisit the problem of supervised learning in temporally coding multilayer spiking neural networks. First, by using a surrogate gradient approach, we derive SuperSpike, a nonlinear voltage-based three-factor learning rule capable of training multilayer networks of deterministic integrate-and-fire neurons to perform nonlinear computations on spatiotemporal spike patterns. Second, inspired by recent results on feedback alignment, we compare the performance of our learning rule under different credit assignment strategies for propagating output errors to hidden units. Specifically, we test uniform, symmetric, and random feedback, finding that simpler tasks can be solved with any type of feedback, while more complex tasks require symmetric feedback. In summary, our results open the door to obtaining a better scientific understanding of learning and computation in spiking neural networks by advancing our ability to train them to solve nonlinear problems involving transformations between different spatiotemporal spike time patterns.

## 1 Introduction

Neurons in biological circuits form intricate networks in which the primary mode of communication occurs through spikes. The theoretical basis for how such networks are sculpted by experience to give rise to emergent computations remains poorly understood. Consequently, building meaningful spiking models of brain-like neural networks in silico is a largely unsolved problem. In contrast, the field of deep learning has made remarkable progress in building nonspiking convolutional networks that often achieve human-level performance at solving difficult tasks (Schmidhuber, 2015; LeCun, Bengio, & Hinton, 2015). Although the details of how these artificial rate–based networks are trained may arguably be different from how the brain learns, several studies have begun to draw interesting parallels between the internal representations formed by deep neural networks and the recorded activity from different brain regions (Yamins et al., 2014; McClure & Kriegeskorte, 2016; McIntosh, Maheswaranathan, Nayebi, Ganguli, & Baccus, 2016; Marblestone, Wayne, & Kording, 2016). A major impediment to deriving a similar comparison at the spiking level is that we currently lack efficient ways of training spiking neural network (SNNs), thereby limiting their applications to mostly small toy problems that do not fundamentally involve spatiotemporal spike time computations. For instance, only recently have some groups begun to train SNNs on data sets such as MNIST (Diehl & Cook, 2015; Guerguiev, Lillicrap, & Richards, 2017; Neftci, Augustine, Paul, & Detorakis, 2016; Petrovici et al., 2017), whereas most previous studies have used smaller artificial data sets.

The difficulty in simulating and training SNNs originates from multiple factors. First, time is an indispensable component of the functional form of a SNN, as even individual stimuli and their associated outputs are spatiotemporal spike patterns rather than simple spatial activation vectors. This fundamental difference necessitates the use of different cost functions from the ones commonly encountered in deep learning. Second, most spiking neuron models are inherently nondifferentiable at spike time, and the derivative of their output with respect to synaptic weights is zero at all other times. Third, the intrinsic self-memory of most spiking neurons introduced by the spike reset is difficult to treat analytically. Finally, credit assignment in hidden layers is problematic for two reasons: (1) it is technically challenging because efficient autodifferentiation tools are not available for most event-based spiking neural network frameworks, and (2) the method of weight updates implemented by the standard backpropagation of error algorithm (Backprop) is thought to be biologically implausible (Grossberg, 1987; Crick, 1989).

Several studies of multilayer networks that build on the notion of feedback alignment (Lillicrap, Cownden, Tweed, & Akerman, 2016) have recently illustrated that the strict requirements imposed on the feedback by backpropagation of error signals can be loosened substantially without a large loss of performance on standard benchmarks like MNIST (Lillicrap et al., 2016; Guergiuev, Lillicrap, & Richards, 2016; Neftci et al., 2016; Baldi, Sadowski, & Lu, 2016; Liao & Carneiro, 2015). While some of these studies have been performed using spiking networks, they still use effectively a rate-based approach in which a given input activity vector is interpreted as the firing rate of a set of input neurons (Eliasmith et al., 2012; Diehl & Cook, 2015; Guergiuev et al., 2016; Neftci et al., 2016; Mesnard, Gerstner, & Brea, 2016). While this approach is appealing because it can often be related directly to equivalent rate-based models with stationary neuronal transfer functions, it also largely ignores the idea that individual spike timing may carry additional information that could be crucial for efficient coding (Thalmeier, Uhlmann, Kappen, & Memmesheimer, 2016; Denève & Machens, 2016; Abbott, DePasquale, & Memmesheimer, 2016; Brendel, Bourdoukan, Vertechi, Machens, & Denéve, 2017) and fast computation (Thorpe, Fize, & Marlot, 1996; Gollisch & Meister, 2008).

In this article, we develop a novel learning rule to train multilayer SNNs of deterministic leaky integrate-and-fire (LIF) neurons on tasks that fundamentally involve spatiotemporal spike pattern transformations. In doing so, we go beyond the purely spatial rate-based activation vectors prevalent in deep learning. We further study how biologically more plausible strategies for deep credit assignment across multiple layers generalize to the enhanced context of more complex spatiotemporal spike pattern transformations.

### 1.1 Prior Work

Supervised learning of precisely timed spikes in single neurons and networks without hidden units has been studied extensively. Pfister, Toyoizumi, Barber, and Gerstner (2006) have used a probabilistic escape rate model to deal with the hard nonlinearity of the spike. Similar probabilistic approaches have also been used to derive spike timing dependent plasticity (STDP) from information-maximizing principles (Bohte & Mozer, 2007; Toyoizumi, Pfister, Aihara, & Gerstner, 2005). In contrast to that, ReSuMe (Ponulak & Kasiński, 2009) and SPAN (Mohemmed, Schliebs, Matsuda, & Kasabov, 2012) are deterministic approaches that can be seen as generalizations of the Widrow-Hoff rule to spiking neurons. In a similar vein, the Chronotron (Florian, 2012) learns precisely timed output spikes by minimizing the Victor-Pupura distance (Victor & Purpura, 1997) to a given target output spike train. Similarly, Gardner and Grüning (2016) and Albers, Westkott, and Pawelzik (2016) have studied the convergence properties of rules that reduce the van Rossum distance by gradient descent. Moreover, Memmesheimer, Rubin, Ölveczky, & Sompolinsky (2014) proposed a learning algorithm that achieves high capacity in learning long, precisely timed spike trains in single units and recurrent networks. The problem of sequence learning in recurrent neural networks has also been studied as a variational learning problem (Brea, Senn, & Pfister, 2013; Jimenez Rezende & Gerstner, 2014) and by combining adaptive control theory with heterogeneous neurons (Gilra & Gerstner, 2017).

Supervised learning in SNNs without hidden units has also been studied for classification problems. For instance, Maass, Natschläger, and Markram (2002) have used the p-delta rule (Auer, Burgsteiner, & Maass, 2008) to train the readout layer of a liquid state machine. Moreover, the tempotron (Gütig & Sompolinsky, 2006; Gütig, 2016), which can be derived as a gradient-based approach (Urbanczik & Senn, 2009), classifies large numbers of temporally coded spike patterns without explicitly specifying a target firing time.

Only a few works have embarked on the problem of training SNNs with hidden units to process precisely timed input and output spike trains by porting backprop to the spiking domain. The main analytical difficulty in these approaches arises from partial derivatives of the form where is the spike train of the hidden neuron and is a hidden weight. SpikeProp (Bohte, Kok, & La Poutre, 2002) sidesteps this problem by defining a differentiable expression on the firing times instead, on which standard gradient descent can be performed. While the original approach was limited to a single spike per neuron, multiple extensions of the algorithm exist, some of which also improve its convergence properties (McKennoch, Liu, & Bushnell, 2006; Booij & tat Nguyen, 2005; Shrestha & Song, 2015, 2017; de Montigny & Mêsse, 2016; Banerjee, 2016). However, one caveat of such spike timing–based methods is that they cannot learn starting from a quiescent state of no spiking, as the spike time is then ill defined. Some algorithms, however, do not suffer from this limitation. For instance, an extension of ReSuMe to multiple layers was proposed (Sporea & Grüning, 2013) in which error signals were backpropagated linearly. More recently, the same group proposed a more principled generalization of Backprop to SNNs in Gardner, Sporea, and Grüning (2015) using a stochastic approach, which can be seen as an extension of Pfister et al. (2006) to multiple layers. In a similar flavor as Fremaux, Sprekeler, and Gerstner (2010), Gardner et al. (2015) substitute the partial derivative of hidden spike trains by a point estimate of their expectation value. Although, theoretically, stochastic approaches avoid problems arising from quiescent neurons, convergence can be slow, and the injected noise may become a major impediment to learning in practice. Instead of approximating partial derivatives of spike trains by their expectation value, in Bohte (2011), the corresponding partial derivative is approximated as a scaled Heaviside function of the membrane voltage. However, due to the use of the Heaviside function, this approach has a vanishing surrogate gradient for subthreshold activations, which limits the algorithm's applicability to cases in which hidden units are not quiescent. Finally, Huh and Sejnowski (2017) proposed another interesting approach in which instead of approximating partial derivatives for a hard spiking nonlinearity, instead a “soft” spiking threshold is used, for which by design, standard techniques of gradient descent are applicable.

In contrast to this previous work, our method permits training multilayer networks of deterministic LIF neurons to solve tasks involving spatiotemporal spike pattern transformations without the need for injecting noise even when hidden units are initially completely silent. To achieve this, we approximate the partial derivative of the hidden unit outputs as the product of the filtered presynaptic spike train and a nonlinear function of the postsynaptic voltage instead of the postsynaptic spike train. In the following section, we explain the details of our approach.

## 2 Derivation of the SuperSpike Learning Rule

Equation 2.5 corresponds to the SuperSpike learning rule for output neuron . However, by redefining the error signal as a feedback signal, we will use the same rule for hidden units as well. Before we move on to testing this learning rule, we first state a few of its noteworthy properties: (1) it has a Hebbian term that combines pre- and postsynaptic activity in a multiplicative manner, (2) the learning rule is voltage based, (3) it is a nonlinear Hebbian rule due to the occurrence of , (4) the causal convolution with acts as an eligibility trace to solve the distal reward problem due to error signals arriving after an error was made (Izhikevich, 2007), and (5) it is a three-factor rule in which the error signal plays the role of a third factor (Frémaux & Gerstner, 2016; Kusmierz, Isomura, & Toyoizumi, 2017). Unlike most existing three-factor rules, however, the error signal is specific to the postsynaptic neuron, an important point that we will return to.

## 3 Methods

We trained networks of spiking LIF neurons using a supervised learning approach that we call SuperSpike. This approach generalizes the backpropagation of error algorithm (Schmidhuber, 2015) as known from the multilayer perceptron to deterministic spiking neurons. Because the partial derivative, and thus the gradient of deterministic spiking neurons, is zero almost everywhere, to make this optimization problem solvable, we introduce a nonvanishing surrogate gradient (Hinton, 2012; Bengio, Léonard, & Courville, 2013) (cf. equation 2.5). All simulations were run with a temporal resolution of 0.1 ms using the Auryn simulation library, which is publicly available (Zenke & Gerstner, 2014).

### 3.1 Neuron Model

### 3.2 Stimulation Paradigms

Depending on the task at hand, we used two types of stimuli. For simulation experiments in which the network had to learn exact output spike times, we used a set of frozen Poisson spike trains as input. These stimuli consisted of a single draw of , where is the number of input units, Poisson spike trains of a given duration. These spike trains were then repeated in a loop and had to be associated with the target spike train, which was consistently aligned to the repeats of the frozen Poisson inputs. For benchmarking and comparison reasons, the stimulus and target spike trains shown in this article are publicly available as part of the Supervised Spiking Benchmark Suite (version 71291ea; Zenke, 2017).

For classification experiments, we used sets of different stimuli. Individual stimuli were drawn as random neuronal firing time offsets from a common stimulus onset time. Stimulus order was chosen randomly and with randomly varying inter-stimulusintervals.

### 3.3 Plasticity Model

In addition to the neuronal dynamics as described in the previous section, the evaluation of equation 2.5 can thus coarsely be grouped as follows: (1) evaluation of presynaptic traces, (2) evaluation of Hebbian coincidence and computation of synaptic eligibility traces, (3) computation and propagation of error signals, and (4) integration of equation 2.5 and weight update. We next describe each part in more detail.

#### 3.3.1 Presynaptic Traces

#### 3.3.2 Hebbian Coincidence Detection and Synaptic Eligibility Traces

To evaluate the Hebbian term, we evaluate the surrogate partial derivative in every time step. For efficiency reasons, we use the partial derivative of the negative half of a fast sigmoid , which does not require the costly evaluation of exponential functions in every time step. Specifically, we compute with , where is the neuronal firing threshold and unless mentioned otherwise.

We compute the outer product between the delayed presynaptic traces and the surrogate partial derivatives in every time step. Here, the delay is chosen such that it offsets the 0.8 ms axonal delay, which spikes acquire during forward propagation. Because the presynaptic traces decay to zero quickly in the absence of spikes, we approximate them to be exactly zero when their numerical value drops below machine precision of . This allows us to speed up the computation of the outer product by skipping these presynaptic indices in the computation.

To implement the synaptic eligibility trace as given by the temporal filter , we filter the values of the Hebbian product term with two exponential filters as in the case of the presynaptic traces . It is important to note, however, that these traces now need to be computed for each synapse , which makes the algorithm scale as for being the number of neurons. This makes it the most obvious target for future optimizations of our algorithm. Biologically, this complexity could be implemented naturally simply because synaptic spines are electrical and ionic compartments in which a concentration transient of calcium or other messengers decays on short timescales. For SuperSpike to function properly, it is important that these transients are long enough to temporally overlap with any causally related error signal . Formally, the duration of the transient in the model is given by the filter kernel shape used to compute the van Rossum distance. We used a double-exponentially filtered kernel with the same shape as a PSP in the model, but other kernels are possible.

#### 3.3.3 Error Signals

We distinguish two types of error signals: output error signals and feedback signals. Output error signals are directly tied to output units for which a certain target signal exists. Their details depend on the underlying cost function we are trying to optimize. Feedback signals are derived from output error signals by sending them back to the hidden units. In this study, we used two slightly different classes of output error signals and three different types of feedback.

At the level of output errors, we distinguish between the cases in which our aim was to learn precisely timed output spikes. In these cases, the output error signals were exactly given by for an output unit . Unless stated otherwise, we chose but normalized to unity. As can be seen from this expression, the error signal vanishes only if the target and the output spike train exactly match with the temporal precision of our simulation. All cost function values were computed online as the root mean square from a moving average with 10 s time constant.

In simulations in which we wanted to classify input spike patterns rather than generate precisely timed output patterns, we introduced some slack into the computation of the error signal. For instance, as illustrated in Figure 5, we gave instantaneous negative error feedback as described by for each erroneous additional spike . However, since for this task we did not want the network to learn precisely timed output spikes, we gave a positive feedback signal only at the end of a miss trial—that is, when a stimulus failed to evoke an output spike during the window of opportunity when it should have (see section 3.2).

#### 3.3.4 Feedback Signals

We investigated different credit assignment strategies for hidden units. To that end, hidden-layer units received one out of three types of feedback (cf. Figure 3b). We distinguish between symmetric, random, and uniform feedback. Symmetric feedback signals were computed in analogy to backprop as the weighted sum of the downstream error signals using the actual feedforward weights . Note that in contrast to backprop, the nonlocal information of downstream activation functions does not appear in this expression, which is closely related to the notion of straight-through estimators (Hinton, 2012; Bengio et al., 2013; Baldi et al., 2016). Motivated by recent results on feedback alignment (Lillicrap et al., 2016), random feedback signals were computed as the random projection , with random coefficients drawn from a normal distribution with zero mean and unit variance. This configuration could be implemented, for instance, by individual neurons sensing differential neuromodulator release from a heterogeneous population of modulatory neurons. Finally, in the case of uniform feedback, all weighting coefficients were simply set to one corresponding closest to a single global third factor distributed to all neurons, akin to a diffuse neuromodulatory signal.

#### 3.3.5 Weight Updates

To update the weights, the time-continuous time series corresponding to the product of error or feedback signal and the synaptic eligibility traces were not directly added to the synaptic weights, but first integrated in a separate variable in chunks of . Specifically, we computed with at each time step. For stimuli exceeding the duration , this can be seen as the continuous time analogue to minibatch optimization. We chose on the order of half a second as a good compromise between computational cost and performance for synaptic updates. At the end of each interval , all weights were updated according to with the per parameter learning rate . In addition, we enforced the constraint for individual weights to remain in the interval . After updating the weights, the variables were reset to zero.

#### 3.3.6 Per Parameter Learning Rates

To facilitate finding the right learning rate and the speed-up training times in our simulations, we implement a per parameter learning rate heuristic. To compute the per-parameter learning rate, in addition to we integrated another auxiliary quantity ). Here ensures a slow decay of for . Consequently, represents an upper estimate of the noncentered second moment of the surrogate gradient for each parameter on the characteristic timescale . With these definitions, the per parameter learning rate was defined as . This choice is motivated by the RMSprop optimizer, which is commonly used in the field of deep learning (Hinton, 2012). However, RMSprop computes a moving exponential average over the . We found that introducing the max function resulted in a similar cost after convergence compared to RMSprop, but rendered training less sensitive to changes in the learning rate while simultaneously yielding excellent convergence times (see Figure 1). We call this slightly modified version “RMaxProp” (compare also AdaMax; Kingma & Ba, 2014). Finally, the parameter was determined by grid search over the values .

#### 3.3.7 Regularization Term

## 4 Numerical Experiments

To test whether equation 2.5 could be used to train a single neuron to emit a predefined target spike pattern, we simulated a single LIF neuron that received a set of 100 spike trains as inputs. The target spike train was chosen as five equidistant spikes over the interval of 500 ms. The inputs were drawn as Poisson spike trains that repeated every 500 ms. We initialized the weights in a regime where the output neuron only showed subthreshold dynamics but did not spike (see Figure 2a). Previous methods, starting from this quiescent state, would require the introduction of noise to generate spiking, which would in turn retard the speed with which precise output spike times could be learned. Finally, weight updates were computed by evaluating the integral in equation 2.5 over a fixed interval and scaling the resulting value with the learning rate (see section 3). After 500 trials, corresponding to 250 s of simulated time, the output neuron had learned to produce the desired output spike train (see Figure 2b). However, fewer trials could generate good approximations to the target spike train (see Figure 2c).

### 4.1 Learning in Multilayer Spiking Neural Networks

Having established that our rule can efficiently transform complex spatiotemporal input spike patterns to precisely timed output spike trains in a network without hidden units, we next investigated how well the same rule would perform in multilayer networks. The form of equation 2.5 suggests a straightforward extension to hidden layers in analogy to backprop. Namely, we can use the same learning rule; equation 2.5, for hidden units, with the modification that becomes a complicated function that depends on the weights and future activity of all downstream neurons. However, this nonlocality in space and time presents serious problems in terms of both biological plausibility and technical feasibility. Technically, this computation requires either backpropagation through time through the PSP kernel or the computation of all relevant quantities online as, for instance, in the case of RTRL. Here, we explore an approach akin to the latter since our specific choice of temporal kernels allows us to compute all relevant dynamic quantities and error signals online (see Figure 3b). In our approach, error signals are distributed directly through a feedback matrix to the hidden-layer units (see Figure 3a). Specifically, this means that the output error signals are propagated neither through the actual or the “soft” spiking nonlinearity. This idea is closely related to the notion of straight-through estimators in machine learning (Hinton, 2012; Bengio et al., 2013; Baldi et al., 2016). We investigated different configurations of the feedback matrix, which can be (1) symmetric (i.e., the transpose of the feedforward weights), as in the case of backprop; (2) random, as motivated by the recent results on feedback alignment (Lillicrap et al., 2016); or (3) uniform, corresponding closest to a single global third factor distributed to all neurons, akin to a diffuse neuromodulatory signal.

We first sought to replicate the task shown in Figure 2, but with the addition of a hidden layer composed of four LIF neurons. Initially, we tested learning with random feedback. To that end, feedback weights were drawn from a zero mean unit variance gaussian, and their value remained fixed during the entire simulation. The synaptic feedforward weights were also initialized randomly at a level at which neither the hidden units nor the output unit fired a single spike in response to the same input spike trains as used before (see Figure 4a). After training the network for 40 s, some of the hidden units had started to fire spikes in response to the input. Similarly, the output neuron had started to fire at intermittent intervals closely resembling the target spike train (not shown). Continued training on the same task for a total of 250 s led to a further refinement of the output spike train and more differentiated firing patterns in a subset of the hidden units (see Figure 4b).

Although we did not restrict synaptic connectivity to obey Dale's principle, in the example with random feedback, all hidden neurons with positive feedback connections ended up being excitatory, whereas neurons with negative feedback weights generally turned out to be inhibitory at the end of training. These dynamics are a direct manifestation of the feedback alignment aspect of random feedback learning (Lillicrap et al., 2016). Because the example shown in Figure 4 does not strictly require inhibitory neurons in the hidden layer, in many cases the neurons with negative feedback remained quiescent or at low activity levels at the end of learning.

Learning was successful for different initial conditions, although the time for convergence to zero cost varied (see Figure 4d). We did encounter a few cases in which the network completely failed to solve the task. These were the cases in which all feedback connections happened to be initialized with a negative value (see Figure 4c). This eventuality could be made very unlikely, however, by increasing in the number of hidden units (see Figure 4c). Other than that, we did not find any striking differences in performance when we replaced the random feedback connections by symmetric (see Figure 4d) or uniform “all one” feedback weights (see Figure 4e).

The previous task was simple enough such that solving it did not require a hidden layer. We therefore investigated whether SuperSpike could also learn to solve tasks that cannot be solved by a network without hidden units. To that end, we constructed a spiking exclusive-or task in which four different spiking input patterns had to be separated into two classes. In this example, we used 100 input units, although the effective dimension of the problem was two by construction. Specifically, we picked three nonoverlapping sets of input neurons with associated fixed random firing times in a 10 ms window. One set was part of all patterns and served as a time reference. The other two sets were combined to yield the four input patterns of the problem. Moreover, we added a second readout neuron each corresponding to one of the respective target classes (see Figure 5a). The input patterns were given in random order as short bouts of spiking activity at random intertrial intervals during which input neurons were firing stochastically at 4 Hz (see Figure 5b). Because of the added noise, we relaxed the requirement for precise temporal spiking and instead required output neurons to spike within a narrow window of opportunity, which was aligned with and outlasted each stimulus by 15 ms. The output error signal was zero unless the correct output neuron failed to fire within the window. In this case, an error signal corresponding to the correct output was elicited at the end of the window. At any time, an incorrect spike triggered immediate negative feedback. We trained the network comparing different types of feedback. A network with random feedback quickly learned to solve this task with perfect accuracy (see Figures 5b and 5c), whereas a network without hidden units was unable to solve the task (see Figure 5d). Perhaps not surprising, networks with symmetric feedback connections also learned the task quickly, and overall their learning curves were more stereotyped and less noisy (see Figure 5e), whereas networks with uniform feedback performed worse on average (see Figure 5f). Overall, these results illustrate that temporally coding spiking multilayer networks can be trained to solve tasks that cannot be solved by networks without hidden layers. Moreover, these results show that random feedback is beneficial over uniform feedback in some cases.

### 4.2 Limits of Learning with Random Feedback

All tasks considered so far were simple enough that they could be solved by most three-layer networks with zero error for all types of feedback signals. We hypothesized that the observed indifference to the type of feedback could be due to the task being too simple. To test whether this picture would change for a more challenging task, we studied a network with 100 output neurons that had to learn a 3.5 second-long complex spatiotemporal output pattern from cyclically repeating frozen Poisson noise (see section 3). Specifically, we trained a three-layer SNN with 100 input, 100 output, and different numbers of hidden neurons (see Figure 6a). Within 1000 s of training with symmetric feedback connections, a network with 32 or more hidden units could learn to emit an output spike pattern that visually matched the target firing pattern (see Figures 6b and 6c). After successful learning, hidden unit activity was irregular and at intermediate firing rates of 10 to 20 Hz with a close to exponential interspike interval distribution (see Figure 6d). However, the target pattern was not learned perfectly, as evidenced by a number of spurious spikes (see Figure 6c) and a nonvanishing van Rossum cost (see Figure 7a).

On the same task, a simulation with random feedback yielded substantially worse performance (see Figures 7a to 7e), and the output pattern became close to impossible to recognize visually (see Figure 7e). As expected, results from uniform feedback were worst (not shown); hence, we do not consider this option in the following. Notably, the random feedback case performs worse than a network that was trained without a hidden layer. Since we observed abnormally high firing rates in hidden-layer neurons in networks trained with random feedback (see Figure 7e), we wondered whether performance could be improved through the addition of a heterosynaptic weight decay which acts as an activity regularizer (see section 3 and appendix A; Zenke et al., 2015). The addition of an activity-dependent heterosynaptic weight decay term to the hidden-layer learning rule notably decreased hidden-layer activity (see Figures 7f and 8), improved learning performance (see Figures 7a and 7c), and increased the visual similarity of the output patterns (see Figure 7f).

However, even this modified learning rule did not achieve comparable performance levels to a symmetric-feedback network. Importantly, for the hidden-layer sizes we tested, random feedback networks did not even achieve the same performance levels as networks without a hidden layer, whereas symmetric feedback networks did (see Figures 7b and 7c). Not surprisingly, networks with wider hidden layers performed superior to networks with fewer hidden units, but networks with random feedback performed consistently worse than their counterparts trained with symmetric feedback (see Figure 7b). Finally, when we trained the network using symmetric feedback with a learning rule in which we disabled the nonlinear voltage dependence by setting the corresponding term to one, the output pattern was degraded (“Symm. linear” in Figure 7g; cf. equation 2.5), but unlike in the random feedback case, most hidden unit firing rates remained low.

These results seem to confirm our intuition that for more challenging tasks, the nonlinearity of the learning rule, firing rate regularization, and nonrandom feedback seem to become more important to achieving good performance on the type of spatiotemporal spike pattern transformation tasks we considered here.

## 5 Discussion

In this article, we have derived a three-factor learning rule to train deterministic multilayer SNNs of LIF neurons. Moreover, we have assessed the impact of different types of feedback credit assignment strategies for the hidden units, notably symmetric, random, and uniform. In contrast to previous work (Pfister et al., 2006; Fremaux et al., 2010; Gardner et al., 2015), we have used a deterministic surrogate gradient approach instead of the commonly used stochastic gradient approximations. By combining this rule with ideas of straight-through estimators (Hinton, 2012; Bengio et al., 2013) and feedback alignment (Lillicrap et al., 2016; Baldi et al., 2016), we could efficiently train and study precisely timed spiking dynamics in multilayer networks of deterministic LIF neurons without relying on the introduction of extraneous and unavoidable noise present in stochastic models, noise that generally impedes the ability to learn precise spatiotemporal spike pattern transformations.

The weight update equation of SuperSpike constitutes a voltage-based nonlinear Hebbian three-factor rule with individual synaptic eligibility traces. Each of these aspects has direct biological interpretations. For instance, a nonlinear voltage dependence has been reported ubiquitously by numerous studies on Hebbian long-term plasticity induction in hippocampus and cortex (Artola, Bröcher, & Singer, 1990; Feldman, 2012). Also, the window of temporal coincidence detection in our model is in good agreement with that of STDP (Feldman, 2012). Moreover, the time course of the eligibility traces could be interpreted as a local calcium transient at the synaptic spine level. Finally, the multiplicative coupling of the error signal with the eligibility trace could arise from neuromodulators (Izhikevich, 2007; Pawlak, Wickens, Kirkwood, & Kerr, 2010; Frémaux & Gerstner, 2016; Kusmierz et al., 2017). However, instead of only one global feedback signal, our work highlights the necessity of a higher-dimensional neuromodulatory or electrical feedback signal for learning potentially with some knowledge of the feedforward pathway. The biological exploration of such intelligent neuromodulation, as well as extensions of our approach to deeper and recurrent SNNs, are left as intriguing directions for future work.

## Appendix: Analytical Motivation for the Regularization Term

The specific choice of the regularizer introduced in equation 3.5 was motivated by previous work on rapid compensatory processes as an effective way to constrain neuronal activity through linear scaling of afferent weights (Oja, 1982; Zenke et al., 2015).

Note that this expression corresponds to the unregularized learning rule, equation 2.5, normalized by a factor defined by the regularization function , equation 3.5, which by definition solely depends on the postsynaptic activity.

## Acknowledgments

We thank Subhy Lahiri and Ben Poole for helpful discussions. F.Z. was supported by the SNSF (Swiss National Science Foundation) and the Wellcome Trust (110124/Z/15/Z). S.G. was supported by the Burroughs Wellcome, Sloan, McKnight, Simons, and James S. McDonnell foundations and the Office of Naval Research.