Von Economo neurons enable reliable social skill acquisition in recurrent spiking neural networks: a computational account with clinical predictions

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.

We investigate how internal representations emerge across hierarchical processing systems by introducing a neuroscience-inspired framework for analyzing deep spiking neural networks (SNN) through the lens of functional connectivity. Drawing on concepts from systems neuroscience and information theory, we form the first-order functionally-connected (1FC) group of a neuron based on its statistically significant pairwise correlations with neurons from the previous layer of a trained SNN architecture. We then track its response properties during inference under various conditions. Our analysis shows that several principles of functional connectivity previously observed in biological cortex are preserved in spiking ResNet architectures. These 1FC ensembles display interesting properties: their aggregate cofiring reliably predicts downstream neuronal responses through a robust, ReLU-like input-output relationship, whose gain scales systematically with ensemble size. Reliable encoding of the presented class emerges only during high 1FC cofiring events, which themselves occur infrequently, indicating that informative representations are concentrated in rare but highly coordinated activity patterns. Under uniform random noise or adversarial perturbations, these response profiles are disrupted, particularly in early and intermediate layers. This enables a targeted high-resolution interrogation at specific nodes and pathways. We showed that the functional connectivity structure is shaped by learning and this structure breaks under weight permutation. These establish 1FC ensembles as a functionally meaningful substrate for input encoding and information transfer, with potential implications in designing targeted fine-grained diagnostics on the information flow.

In-context learning (ICL) operates via implicit gradient descent embedded in the forward pass of modern AI architectures -- Transformers, Mamba, state-space models, and MLPs. Capturing this capability in biologically plausible Spiking Neural Networks (SNNs) has remained an open challenge: existing SNNs fail the Garg-2022 benchmark at non-trivial task dimensions. We trace this failure to a structural assumption: prior SNN designs route adaptation through inference-time synaptic plasticity, viewing the dendritic compartment as a passive conduit for error or teacher signals. We challenge this assumption. The subthreshold dynamics of a single dendritic compartment already implement a complete online learning algorithm. By treating the compartment as the computational substrate rather than a passive conduit, we propose DendriCL -- a single-layer compartmental spiking architecture whose apical recurrence is structurally identical to leaky online Widrow-Hoff LMS. This dynamics-only update collapses the architectural depth required for general-purpose ICL to a single layer. DendriCL is uniquely seed-stable at super-dimensional Garg-2022 ICL -- where dense Transformers exhibit grokking-style instability and fail past moderate task dimension -- and a linear probe recovers the reference online-LMS trajectory directly from the apical membrane at R^2 = 0.93, showing the algorithm is structurally embedded in the dynamics rather than implicitly discovered during training. Taken together, ICL requires neither attention, depth, nor inference-time plasticity: a single compartment with online-LMS dynamics is sufficient.