Quantifying the distribution of feature values over data represented in arbitrary dimensional spaces.

Identifying the structured distribution (or lack thereof) of a given feature over a point cloud is a general research question. In the neuroscience field, this problem arises while investigating representations over neural manifolds (e.g., spatial coding), in the analysis of neurophysiological signals (e.g., sensory coding) or in anatomical image segmentation. We introduce the Structure Index (SI) as a directed graph-based metric to quantify the distribution of feature values projected over data in arbitrary D-dimensional spaces (defined from neurons, time stamps, pixels, genes, etc). The SI is defined from the overlapping distribution of data points sharing similar feature values in a given neighborhood of the cloud. Using arbitrary data clouds, we show how the SI provides quantification of the degree and directionality of the local versus global organization of feature distribution. SI can be applied to both scalar and vectorial features permitting quantification of the relative contribution of related variables. When applied to experimental studies of head-direction cells, it is able to retrieve consistent feature structure from both the high- and low-dimensional representations, and to disclose the local and global structure of the angle and speed represented in different brain regions. Finally, we provide two general-purpose examples (sound and image categorization), to illustrate the potential application to arbitrary dimensional spaces. Our method provides versatile applications in the neuroscience and data science fields.

Topological analysis of sharp-wave ripple waveforms reveals input mechanisms behind feature variations.

The reactivation of experience-based neural activity patterns in the hippocampus is crucial for learning and memory. These reactivation patterns and their associated sharp-wave ripples (SWRs) are highly variable. However, this variability is missed by commonly used spectral methods. Here, we use topological and dimensionality reduction techniques to analyze the waveform of ripples recorded at the pyramidal layer of CA1. We show that SWR waveforms distribute along a continuum in a low-dimensional space, which conveys information about the underlying layer-specific synaptic inputs. A decoder trained in this space successfully links individual ripples with their expected sinks and sources, demonstrating how physiological mechanisms shape SWR variability. Furthermore, we found that SWR waveforms segregated differently during wakefulness and sleep before and after a series of cognitive tasks, with striking effects of novelty and learning. Our results thus highlight how the topological analysis of ripple waveforms enables a deeper physiological understanding of SWRs.

From cell types to population dynamics: Making hippocampal manifolds physiologically interpretable.

The study of the hippocampal code is gaining momentum. While the physiological approach targets the contribution of individual cells as determined by genetic, biophysical and circuit factors, the field pushes for a population dynamic approach that considers the representation of behavioural variables by a large number of neurons. In this alternative framework, neuronal activity is projected into low-dimensional manifolds. These manifolds can reveal the structure of population representations, but their physiological interpretation is challenging. Here, we review the recent literature and propose that integrating information regarding behavioral traits, local field potential oscillations and cell-type-specificity into neural manifolds offers strategies to make them interpretable at the physiological level.

Deep learning-based feature extraction for prediction and interpretation of sharp-wave ripples in the rodent hippocampus.

Local field potential (LFP) deflections and oscillations define hippocampal sharp-wave ripples (SWRs), one of the most synchronous events of the brain. SWRs reflect firing and synaptic current sequences emerging from cognitively relevant neuronal ensembles. While spectral analysis have permitted advances, the surge of ultra-dense recordings now call for new automatic detection strategies. Here, we show how one-dimensional convolutional networks operating over high-density LFP hippocampal recordings allowed for automatic identification of SWR from the rodent hippocampus. When applied without retraining to new datasets and ultra-dense hippocampus-wide recordings, we discovered physiologically relevant processes associated to the emergence of SWR, prompting for novel classification criteria. To gain interpretability, we developed a method to interrogate the operation of the artificial network. We found it relied in feature-based specialization, which permit identification of spatially segregated oscillations and deflections, as well as synchronous population firing typical of replay. Thus, using deep learning-based approaches may change the current heuristic for a better mechanistic interpretation of these relevant neurophysiological events.

Artificial intelligence is finding greater use in society through its ability to process data in new ways. One particularly useful approach known as convolutional neural networks is typically used for image analysis, such as face recognition. This type of artificial intelligence could help neuroscientists analyze data produced by new technologies that record brain activity with higher resolution. Advanced processing could potentially identify events in the brain in real-time. For example, signals called sharp-wave ripples are produced by the hippocampus, a brain region involved in forming memories. Detecting and interacting with these events as they are happening would permit a better understanding of how memory works. However, these signals can vary in form, so it is necessary to detect several distinguishing features to recognize them. To achieve this, Navas-Olive, Amaducci et al. trained convolutional neural networks using signals from electrodes placed in a region of the mouse hippocampus that had already been analyzed, and 'telling' the neural networks whether they got their identifications right or wrong. Once the networks learned to identify sharp-wave ripples from this data, they could then apply this knowledge to analyze other recordings. These included datasets from another part of the mouse hippocampus, the rat brain, and ultra-dense probes that simultaneously assess different brain regions. The convolutional networks were able to recognize sharp-wave ripple events across these diverse circumstances by identifying unique characteristics in the shapes of the waves. These results will benefit neuroscientists by providing new tools to explore brain signals. For instance, this could allow them to analyze the activity of the hippocampus in real-time and potentially discover new aspects of the processes behind forming memories.