Optimal Decoding of Neural Dynamics Occurs at Mesoscale Spatial and Temporal Resolutions

IntroductionUnderstanding the neural code has been one of the central aims of neuroscience research for decades. Spikes are commonly referred to as the units of information transfer, but multi-unit activity (MUA) recordings are routinely analyzed in aggregate forms such as binned spike counts, peri-stimulus time histograms, firing rates, or population codes. Various forms of averaging also occur in the brain, from the spatial averaging of spikes within dendritic trees to their temporal averaging through synaptic dynamics. However, how these forms of averaging are related to each other or to the spatial and temporal units of information representation within the neural code has remained poorly understood. Materials and MethodsIn this work we developed NeuroPixelHD, a symbolic hyperdimensional model of MUA, and used it to decode the spatial location and identity of static images shown to n = 9 mice in the Allen Institute Visual Coding - NeuroPixels dataset from large-scale MUA recordings. We parametrically varied the spatial and temporal resolutions of the MUA data provided to the model, and compared its resulting decoding accuracy. ResultsFor almost all subjects, we found 125ms temporal resolution to maximize decoding accuracy for both the spatial location of Gabor patches (81 classes for patches presented over a 9x9 grid) as well as the identity of natural images (118 classes corresponding to 118 images). The optimal spatial resolution was more heterogeneous among subjects, but was still found at either of two mesoscale levels in nearly all cases: the area level, where the spiking activity of neurons within each brain area are combined, and the population level, where the former are aggregated into two variables corresponding to fast spiking (putatively inhibitory) and regular spiking (putatively excitatory) neurons, respectively. DiscussionOur findings corroborate existing empirical practices of spatiotemporal binning and averaging in MUA data analysis, and provide a rigorous computational framework for optimizing the level of such aggregations. Our findings can also synthesize these empirical practices with existing knowledge of the various sources of biological averaging in the brain into a new theory of neural information processing in which the unit of information varies dynamically based on neuronal signal and noise correlations across space and time.