BCCN Munich lecture series

We hardly notice when there is a speck on our glasses, the obstructed visual information seems to be magically filled in. The visual system uses visual context to predict the content of the stimulus. What enables neurons in the visual system to respond to context when the stimulus is not available? In cortex, sensory processing is based on a combination of feedforward information arriving from sensory organs, and feedback information that originates in higher-order areas. Whereas feedforward information drives the activity in cortex, feedback information is thought to provide contextual signals that are merely modulatory. We have made the exciting discovery that mouse primary visual cortical neurons are strongly driven by feedback projections from higher visual areas, in particular when their feedforward sensory input from the retina is missing. This drive is so strong that it makes visual cortical neurons fire as much as if they were receiving a direct sensory input.

The processing of temporal sound features is fundamental to hearing, and the auditory system displays a plethora of specializations, at many levels, to enable such processing. Octopus neurons are the most extreme temporally-specialized cells in the auditory (and perhaps entire) brain, which make them intriguing but also difficult to study. Notwithstanding the scant physiological data, these neurons have been a favorite cell type of modeling studies which have proposed that octopus cells have critical roles in pitch and speech perception. We used a range of in vivo recording and labeling methods to examine the hypothesis that tonotopic ordering of cochlear afferents combines with dendritic delays to compensate for cochlear delay - which would explain the highly entrained responses of octopus cells to sound transients. Unexpectedly, the experiments revealed that these neurons have marked selectivity to the direction of fast frequency glides, which is tied in a surprising way to intrinsic membrane properties and subthreshold events. The data suggest that octopus cells have a role in temporal comparisons across frequency and may play a role in auditory scene analysis.

Threshold-linear networks (TLNs) display a wide variety of nonlinear dynamics including multistability, limit cycles, quasiperiodic attractors, and chaos. Over the past few years, we have developed a detailed mathematical theory relating stable and unstable fixed points of TLNs to graph-theoretic properties of the underlying network. In particular, we have discovered that a special type of unstable fixed points, corresponding to "core motifs," are predictive of dynamic attractors. Recently, we have used these ideas to classify dynamic attractors in a two-parameter family of inhibition-dominated TLNs spanning all 9608 directed graphs of size n=5. Remarkably, we find a striking modularity in the dynamic attractors, with identical or near-identical attractors arising in networks that are otherwise dynamically inequivalent. This suggests that, just as one can store multiple static patterns as stable fixed points in a Hopfield model, a variety of dynamic attractors can also be embedded in a TLN in a modular fashion.

A central question in motor physiology has been whether motor cortex activity resembles muscle activity, and if not, why not? Over fifty years, extensive observations have failed to provide a concise answer, and the topic remains much debated. To provide a different perspective, we employed a novel behavioral paradigm that affords extensive comparison between time-evolving neural and muscle activity. Single motor-cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid ’trajectory tangling’: moments where similar activity patterns led to dissimilar future patterns. Avoidance of trajectory tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Remarkably, we were able to predict motor cortex activity from muscle activity alone, by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling. Our results argue that motor cortex embeds descending commands in additional structure that ensure low tangling, and thus noise-robustness. The dominant structure in motor cortex may thus serve not a representational function (encoding specific variables) but a computational function: ensuring that outgoing commands can be generated reliably. Our results establish the utility of an emerging approach: understanding the structure of neural activity based on properties of population geometry that flow from normative principles such as noise robustness.

Cortical circuits receive multiple inputs from upstream populations with non-overlapping stimulus tuning preferences. Both the feedforward and recurrent architectures of the receiving cortical layer will reflect this diverse input tuning. We study how population-wide neuronal variability propagates through a hierarchical cortical network receiving multiple, independent, tuned inputs. We present new analysis of in vivo neural data from the primate visual system showing that the number of latent variables (dimension) needed to describe population shared variability is smaller in V4 populations compared to those of its downstream visual area PFC. We successfully reproduce this dimensionality expansion from our V4 to PFC neural data using a multi-layer spiking network with structured, feedforward projections and recurrent assemblies of multiple, tuned neuron populations. We show that tuning-structured connectivity generates attractor dynamics within the recurrent PFC current, where attractor competition is reflected in the high dimensional shared variability across the population. Indeed, restricting the dimensionality analysis to activity from one attractor state recovers the low-dimensional structure inherited from each of our tuned inputs. Our model thus introduces a framework where high-dimensional cortical variability is understood as ``time-sharing’’ between distinct low-dimensional, tuning-specific circuit dynamics.