Learning place cells, grid cells and invariances with excitatory and inhibitory plasticity

Abstract

Neurons in the hippocampus and adjacent brain areas show a large diversity in their tuning to location and head direction, and the underlying circuit mechanisms are not yet resolved. In particular, it is unclear why certain cell types are selective to one spatial variable, but invariant to another. For example, place cells are typically invariant to head direction. We propose that all observed spatial tuning patterns – in both their selectivity and their invariance – arise from the same mechanism: Excitatory and inhibitory synaptic plasticity driven by the spatial tuning statistics of synaptic inputs. Using simulations and a mathematical analysis, we show that combined excitatory and inhibitory plasticity can lead to localized, grid-like or invariant activity. Combinations of different input statistics along different spatial dimensions reproduce all major spatial tuning patterns observed in rodents. Our proposed model is robust to changes in parameters, develops patterns on behavioral timescales and makes distinctive experimental predictions.

eLife digest

Knowing where you are never hurts, be it during a holiday in New York or on a hiking trip in the Alps. Our sense of location seems to depend on a structure deep within the brain called the hippocampus, and its neighbor, the entorhinal cortex. Studies in rodents have shown that these areas act a little like an in-built GPS for the brain. They contain different types of neurons that help the animal to work out where it is and where it is going. Among those are place cells, present within the hippocampus, and grid cells and head direction cells, found within the entorhinal cortex and other areas.

Place cells fire whenever an animal occupies a specific location in its environment, with each place cell firing at a different spot. Grid cells generate virtual maps of the surroundings that resemble grids of repeating triangles. Whenever an animal steps onto a corner of one of these virtual triangles, the grid cell that generated that map starts to fire. Head direction cells increase their firing whenever an animal’s head is pointing in a specific direction. These cell types thus provide animals with complementary information about their location. But how do the cells first become selective for specific places or head directions?

Weber and Sprekeler propose that a single mechanism gives rise to the spatial characteristics of all these different types of cells. Like all neurons, these cells communicate with their neighbors at junctions called synapses. These may be either excitatory or inhibitory. Cells at excitatory synapses activate their neighbors, whereas cells at inhibitory synapses deactivate them. Weber and Sprekeler used a computer to simulate changes in excitatory and inhibitory synapses in a virtual rat exploring an environment. Interactions between the two types of synapses gave rise to virtual cells that behaved like place, grid or head direction cells. Which cell type emerged depended on whether the excitatory or the inhibitory synapses were more sensitive to the virtual rat’s location.

This idea adds to a range of others proposed to explain how the brain codes for locations. Whether any of these ideas or a combination of them is correct remains to be determined. Further pieces are needed if we are to solve the puzzle of how the brain supports navigation.