My group pioneered the development of a novel intracortical brain computer interface (iBCI) that decodes muscle activity (EMG) from signals recorded in the motor cortex of animals. We use these synthetic EMG signals to control Functional Electrical Stimulation (FES), which causes the muscles to contract and thereby restores rudimentary voluntary control of the paralyzed limb. In the past few years, there has been much interest in the fact that information from the millions of neurons active during movement can be reduced to a small number of “latent” signals in a low-dimensional manifold computed from the multiple neuron recordings. These signals can be used to provide a stable prediction of the animal’s behavior over many months-long periods, and they may also provide the means to implement methods of transfer learning across individuals, an application that could be of particular importance for paralyzed human users. We have begun to examine the representation within this latent space, of a broad range of behaviors, including well-learned, stereotyped movements in the lab, and more natural movements in the animal’s home cage, meant to better represent a person’s daily activities. We intend to develop an FES-based iBCI that will restore voluntary movement across a broad range of motor tasks without need for intermittent recalibration. However, the nonlinearities and context dependence within this low-dimensional manifold present significant challenges.

The head direction (HD) system is classically modeled as a ring attractor network which ensures a stable representation of the animal’s head direction. This unidimensional description popularized the view of the HD system as the brain’s internal compass. However, unlike a globally consistent magnetic compass, the orientation of the HD system is dynamic, depends on local cues and exhibits remapping across familiar environments5. Such a system requires mechanisms to remember and align to familiar landmarks, which may not be well described within the classic 1-dimensional framework. To search for these mechanisms, we performed large population recordings of mouse thalamic HD cells using calcium imaging, during controlled manipulations of a visual landmark in a familiar environment. First, we find that realignment of the system was associated with a continuous rotation of the HD network representation. The speed and angular distance of this rotation was predicted by a 2nd dimension to the ring attractor which we refer to as network gain, i.e. the instantaneous population firing rate. Moreover, the 360-degree azimuthal profile of network gain, during darkness, maintained a ‘memory trace’ of a previously displayed visual landmark. In a 2nd experiment, brief presentations of a rotated landmark revealed an attraction of the network back to its initial orientation, suggesting a time-dependent mechanism underlying the formation of these network gain memory traces. Finally, in a 3rd experiment, continuous rotation of a visual landmark induced a similar rotation of the HD representation which persisted following removal of the landmark, demonstrating that HD network orientation is subject to experience-dependent recalibration. Together, these results provide new mechanistic insights into how the neural compass flexibly adapts to environmental cues to maintain a reliable representation of the head direction.