Brain's GPS never stops working -- even during sleep

The neuronal compass is activated in an organized manner during sleep, exactly as if animals were awake. This demonstrates that the system is hard-wired in such a way that it provides the navigation system with a reliable and unambiguous signal at all times.

HFSP Long-Term Fellow Adrien Peyrache and Program Grant holder György Buzsáki and colleagues
authored on Thu, 21 May 2015

Have you ever felt a whirling sensation as if the world is spinning after just realizing you were lost in a city you were visiting for the first time? This happens when the neuronal circuits in your brain that allow you to navigate the world suddenly lose their confidence in the estimation of your location. Fortunately, this brain system excels in familiar environments, and can rapidly adapt to modifications, allowing you, for example, to easily make a detour when a street is blocked by construction vehicles while on your way to work. We are interested in determining the physiological basis of our brain’s internal representation of our location in space, and how adaptive processes can take place when a familiar representation is challenged.

Figure: Persistence of head-direction cell assemblies during waking and sleep. WAKING: simultaneously recorded head-direction cells with different direction preferences during exploration (right). Each line is a neuron, increasing firing rates are represented by hot colors. Neurons are ordered according to their preferred head-direction. Note sequential activity of head-direction neurons (from top to bottom). (Left) Head-direction cell assembly activity displayed on a ring. As the head points to different directions, the hill of spiking activity moves on the ring accordingly. SLEEP: same arrangement as in waking. Note continued sequentially changing activity of the head-direction cells despite the absence of head or body movement.

Navigating and locating oneself in the environment is a matter of survival for all animals. Finding food and shelter are two obvious examples of this need. Highly sophisticated brain circuits which developed early on during evolution enable animals to roam over large distances for long periods of time, yet retain the ability to return home along the most straightforward path on demand. When visual, or other external sensory information is not accessible, the brain's internal navigational system relies on a parallel circuitry which is primarily updated by internal signals. Sailors in the XVth century used dead reckoning navigation in such conditions: they realized that it was enough to know your current direction and speed to update the estimate of one's position in the open sea. The brain does the same: the vestibular system, located in the inner ears, is a remarkable biological gyroscope which tells your brain at what speed your head is moving. Quite amazingly, there is an assembly of neurons that act as a compass and provide the navigation system with an estimate of the current direction of the head, even in pitch dark. They are the so-called head-direction (HD) cells discovered about 30 years ago. One important constraint is that, at any time, the neuronal compass should exhibit one and only one “needle”: these neurons have thus been hypothesized to be wired such that only one subset of HD cells is allowed to fire at any given time, together representing the current head direction.

Leveraging cutting-edge techniques which enable the monitoring of large (>100) ensembles of neurons in freely moving animals, we tested the following key prediction: if the system is wired as described above, the same neuronal activity dynamics should be observable during sleep. To our great surprise, this is exactly what we found. These HD cells continue to fire in an organized manner during sleep, exactly as if animals were awake. However, instead of always pointing towards the same direction - the animals are asleep and thus immobile - the neuronal needle moves constantly. In particular, during Rapid Eye Movement sleep, a brain state rich in dreaming activity in humans and whose electrical activity is virtually indistinguishable from the waking brain, this needle moves exactly as if the animal was awake. HD neurons are sequentially activated and the individual neurons representing a common direction during waking are still active, or silent, at the same time.

These findings thus indicate that the neurons underlying the sense of head direction do not just passively relay vestibular signals. On the contrary, they are endowed with internal properties which enhance the precision of the signal. In particular, it seems that they are hard wired in such a way that they convey an unambiguous and reliable signal to the navigational system in downstream structures, at all times, even in the absence of true sensory information.

Reference

Internally organized mechanisms of the head direction sense. Adrien Peyrache, Marie M Lacroix, Peter C Petersen, György Buzsáki (2015) Nature Neuroscience 18(4):569-75. doi: 10.1038/nn.3968.

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