Sense of direction

Internally organised mechanisms of the head direction sense

Adrien Peyrache, Marie Lacroix, Peter Petersen, Gyorgy Buzsaki, The Neuroscience Institute, University of New York  ::  Nature Neuroscience, Vol. 18, No. 4, April 2015  ::

Summary and review of the above article

Head-direction systems function as a compass. Neurons involved in these systems increase their firing rates when the head is pointed in a particular direction. Firing is also influenced by the angular velocity of head momentum. F9_largeHead-direction information is viewed as a key part of the brain’s navigation system, and is also important for the development of grid cells in the entorhinal cortex.

Internal networks

Head-direction networks have been suggested to represent orientation, being achieved by means of internal network interactions. Head-direction neurons in multiple brain regions maintain a representation of a subject’s direction. Individual neurons are tuned to particular directions, and the subset of neurons active at any particular moment represents the subject’s direction.

Ring attractors

Since the 1990s, theorists have proposed an attractor network or ring attractor of neurons that function together, keeping the representation of direction aligned, or recovering it, in the case of the subject becoming disoriented. Neurons not orientated to a particular direction are suggested to be inhibited, giving local excitations surrounded by global inhibition. In contrast to a compass that selects an external north, the head-direction system defines its own ‘north’. The location of activity on the ‘ring’ differentiates the subject’s direction. The internal generation of direction is thus a type of internal neural compass driven by the activity of specific neurons. The internal processing is seen as the primary factor with external signals then becoming associated with it.

Neural recordings

The authors discuss the extent to which head-direction processes depend on internally generated activity, and the extent to which they depend on external signals. The relationship between internally generated activity and external signals is a key topic in current neuroscience. The authors’ study was based on recordings of the activity of ensembles of head-direction neurons in the antero-dorsal thalamic nucleus and the post-subiculum. biosensors-04-00221-g003-1024Their findings show that external inputs, including visual signals, influence an internally organised network that enhances such signals. The head-direction system involves multiple brain regions including the brain stem, the antero-dorsal thalamic nucleus, the post-subiculum and the entorhinal cortex.

Preservation in sleep

The coherence of the head-direction neurons was preserved in sleep indicating that the connectivity of the head-direction neurons is sustained in sleep. This finding has been seen to confirm the existence of internally generated head-direction. The much faster timescale during slow wave sleep was seen as being reminiscent of hippocampal signalling during sleep.

The study found that the correlated activity of the antero-dorsal nucleus and the post-subiculum was preserved across different brain states, and appeared to derive from a combination of internal and external processes. In sleep, the head-direction system can move independently of sensory inputs, thus indicating an internally organised aspect that makes predictions, which can subsequently be combined with external signals, and adapted to ongoing changes in the environment. With ambiguous external signals, internal head-direction systems may help resolve conflicts in navigational decisions.

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