Teaching signal synchronization in deep neural networks with prospective neurons
Authors: Nicolas Zucchet, Qianqian Feng, Axel Laborieux, Friedemann Zenke, Walter Senn, João Sacramento
Abstract
Working memory requires the brain to maintain information from the recent past to guide ongoing behavior. Neurons can contribute to this capacity by slowly integrating their inputs over time, creating persistent activity that outlasts the original stimulus. However, when these slowly integrating neurons are organized hierarchically, they introduce cumulative delays that create a fundamental challenge for learning: teaching signals that indicate whether behavior was correct or incorrect arrive out-of-sync with the neural activity they are meant to instruct. Here, we demonstrate that neurons enhanced with an adaptive current can compensate for these delays by responding to external stimuli prospectively -- effectively predicting future inputs to synchronize with them. First, we show that such prospective neurons enable teaching signal synchronization across a range of learning algorithms that propagate error signals through hierarchical networks. Second, we demonstrate that this successfully guides learning in slowly integrating neurons, enabling the formation and retrieval of memories over extended timescales. We support our findings with a mathematical analysis of the prospective coding mechanism and learning experiments on motor control tasks. Together, our results reveal how neural adaptation could solve a critical timing problem and enable efficient learning in dynamic environments.
Human cognition emerges from coordinated spiking dynamics in distributed neural circuits, where information is encoded via both firing rates and precise spike timing determined by brain rhythms. Inspired by this notion, we propose a brain-inspired learning primitive in which cognition-level neural synchrony emerges through iterative bottom-up and top-down interactions between micro-scale dynamics of spiking neurons and a macro-scale mechanism of oscillatory synchronization. Specifically, we model each parcel (e.g., a cortical region or an image pixel) in the target system as a spiking neuron embedded in a predefined connectivity scaffold. Low-level information is encoded in a spatiotemporal domain, where neurons are selectively grouped and fire spontaneously over time through self-organized dynamics. In the bottom-up route, oscillatory synchronization is formed from past spiking activity accumulated over a finite memory window. Since brain dynamics operate in a regime of partial and transient synchronization rather than global phase locking, we model oscillatory coordination using a time-delayed synchronization formulation, which enables a top-down modulation of heterogeneous neural spiking for a large-scale distributed system. Together, we devise a spiking-by-synchronization neural network (S2-Net) that uses rhythmic timing as a control mechanism for efficient information processing. Promising results have been achieved across a broad range of tasks, including neural activity decoding, energy-efficient signal processing, temporal binding and semantic reasoning.
The brain uses discrete spikes for dynamic computation, yet, how neural microcircuits (NMCs) solve temporal credit assignment using local spike timing remains a fundamental open question. Dominant spiking neural network (SNN) approaches circumvent this by approximating backpropagation through surrogate gradients, decoupling learning from biological spike timing. Here, we reformulate temporal credit assignment as a state separation problem: extracting task-required components induced by historical perturbations directly from the current neural state. This enables an online feedback learning framework for NMCs through a gradient tunneling (GT) algorithm and the lead-lag expansion technique that derives credit assignment from local synaptic spike timing, while remaining compatible with ANN-SNN hybrid architectures. Experimentally, GT-trained NMCs excel at long-timescale evidence integration and noise-robust memory retention, and perform comparably to leading SNN online learning methods on real-world benchmarks with far fewer parameters. The proposed framework addresses the two-decade-old NMC feedback learning problem and suggests a computationally plausible explanation for the brain's learning mechanisms.
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.