Diffusing Blame: Task-Dependent Credit Assignment in Biologically Plausible Dual-Stream Networks
Authors: Yutaro Yamada, Luca Grillotti, Rujikorn Charakorn, Sebastian Risi, David Ha, Robert Tjarko Lange
Organizations: Sakana AI
Abstract
Biological neural circuits obey Dale's principle: each neuron's synapses are uniformly excitatory or inhibitory. Artificial networks that respect this constraint must coordinate separate excitatory and inhibitory populations, fundamentally changing how credit is assigned during learning. Several biologically plausible learning rules avoid backpropagation's weight transport requirement, but it has been difficult to achieve strong performance under Dale's principle beyond MNIST. Error Diffusion (ED) was originally proposed in a dual-stream excitatory/inhibitory architecture, where learning is driven by routing global error signals to all layers without transporting transposed forward weights or relying on random feedback matrices. Whether such a rule can scale under Dale's principle across both supervised classification and reinforcement learning remains unknown. Here, we introduce modulo error routing to extend Error Diffusion beyond binary classification, and show that a dual-stream excitatory/inhibitory architecture trained with this method achieves 96.7% on MNIST and establishes a 61.7% baseline on CIFAR-10, demonstrating that representation learning is possible even when strictly enforcing Dale's principle. For the classification setting, we introduce three domain-specific innovations: layer-specific sigmoid widths, batch-centered class error signals, and asymmetric initialization, and ablation analysis reveals that their relative importance reverses between MNIST and CIFAR-10, exposing task-dependent credit-assignment bottlenecks invisible to single-benchmark evaluation. In reinforcement learning, we integrate ED with Proximal Policy Optimization (PPO) and evaluate it on continuous-control tasks in Google Brax and on Craftax, an open-ended exploration task. We show that ED-PPO achieves competitive performance relative to Direct Feedback Alignment, a backpropagation-free baseline.
Biologically plausible learning models aim to explain how neural circuits can implement effective learning under the constraints of real neurons. Although significant progress has been made, a major remaining challenge is that existing models often allow neurons or synapses to represent mixed-sign values, both positive and negative, in violation of a basic aspect of cortical circuitry -- Dale's constraint: biological neurons are either excitatory or inhibitory, but not both, and synapses cannot change sign. In this work, we address this discrepancy by introducing a biologically motivated neural architecture in which both neural activations and learning signals are represented by non-negative activity, and synapses have fixed sign, while still supporting backpropagation-like learning. Our approach uses two complementary interacting non-negative channels to represent positive and negative contributions, inspired by evidence of on-off representations in the brain. These channels are implemented through a simple neural circuit motif, which is repeated throughout the network in both bottom-up and top-down pathways. Combined with a local Hebbian learning rule, the resulting model propagates learning signals and updates weights using only local interactions between neurons. We show theoretically that our learning scheme can exactly recover the backpropagation update despite relying solely on non-negative error signals. Empirically, beyond satisfying stronger biological constraints, the on-off architecture learns efficient representations, yielding substantial gains over comparable vanilla networks on the Tiny ImageNet benchmark. These results demonstrate that effective learning can emerge from biologically plausible mechanisms without requiring mixed-sign signals, providing a step toward more realistic models of neural computation.
We introduce Score Broadcast and Decorrelation (SBD), a principled framework for broadcast-based credit assignment for general families of differentiable losses. Error broadcast is a biologically plausible alternative to backpropagation that sends output information to hidden layers without weight transport. The Error Broadcast and Decorrelation (EBD) framework, recently introduced for the mean-squared-error (MSE) setting, grounded this mechanism in the stochastic orthogonality of optimal estimators, under which the optimal residual is orthogonal to functions of the input. We generalize that foundation by introducing an orthogonality principle between the output score (the gradient of loss with respect to the final-layer output) and hidden-layer activations, which holds whenever the optimal score has conditional mean zero. This single principle unifies broadcast-based credit assignment across the standard differentiable-loss families, including cross-entropy, Bregman divergences, proper scoring rules, and exponential-family negative log-likelihoods. The framework supplies a theoretical grounding for the three-factor learning rule under general losses, with the neuromodulatory factor derived as the broadcast loss score. We derive the cross-entropy case explicitly, characterize the admissible loss class, and introduce a score vector expansion technique that enriches the broadcast signal while preserving the orthogonality framework. Experiments on CIFAR-10 and Tiny ImageNet show that SBD substantially improves over existing broadcast approaches, with score vector expansion delivering further gains. Overall, this work identifies the loss score as the signal to broadcast, supplies the orthogonality theory and theoretical grounding for the three-factor learning rule from neuroscience, and shows how score vector expansion enriches the decorrelation directions of the resulting objective.
Modern machine learning applications employ deep neural networks training with the error backpropagation algorithm. Although this algorithm is very effective, it lacks biological realism. For example, backpropagation requires symmetric connectivity, and a separate neural processing channel for error signals. Prior works have therefore proposed a number of more realistic alternatives for error backpropagation. However, most of them still suffer from demanding preassumptions that may be not fulfilled in the real brain, for example, they often still require either symmetric connectivity or two separate processing channels, and often require also special mathematical operations like subtractions or function inversions. Here I propose supervised counterstream learning in deep associative networks as a simpler approach that requires only recognition of errors during training, and then backpropagates correcting target activity through the same activity channel as used for forward propagation. For this, two activity waves are initiated at the same time in input and output layers and then traveling in opposite directions to meet in one of the hidden layers. By employing simple local Hebbian-type learning rules, the corresponding activity pattern sequences get linked bidirectionally, thereby decreasing error rates over time. Despite its simplicity and an incomplete hyperparameter optimzation, a high high test accuracy is achieved on the (binarized) MNIST data set that is comparable to more demanding architectures.