Abstract

How the brain combines information from different sensory modalities and of differing reliability is an important and still-unanswered question. Using the head direction (HD) system as a model, we explored the resolution of conflicts between landmarks and background cues. Sensory cue integration models predict averaging of the two cues, whereas attractor models predict capture of the signal by the dominant cue. We found that a visual landmark mostly captured the HD signal at low conflicts: however, there was an increasing propensity for the cells to integrate the cues thereafter. A large conflict presented to naive rats resulted in greater visual cue capture (less integration) than in experienced rats, revealing an effect of experience. We propose that weighted cue integration in HD cells arises from dynamic plasticity of the feed-forward inputs to the network, causing within-trial spatial redistribution of the visual inputs onto the ring. This suggests that an attractor network can implement decision processes about cue reliability using simple architecture and learning rules, thus providing a potential neural substrate for weighted cue integration.

Highlights

  • The ‘sense of direction’ is supported by the limbic head direction (HD) cells, which respond to allocentric HD regardless of the animal’s location in an environment [1,2]

  • The present experiment examined how HD cells responded to a conflict between two cue sets: background cues versus a highly salient landmark cue

  • We found that the cells responded not by ‘cue capture’, a winner-take-all process in which they followed the strongest cue set, but rather in an integrative fashion in which the cells adopted a firing direction intermediate between the directions signalled by the two cue sets

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Summary

Introduction

The ‘sense of direction’ is supported by the limbic head direction (HD) cells, which respond to allocentric HD (that is, direction of the head with respect to the world) regardless of the animal’s location in an environment [1,2]. When a well-isolated and stable HD cell was found, the rat was taken into the experimental room in an opaque carrying box and placed on a raised holding box outside the curtained enclosure, in order to acclimatize to the room for 5 min During this time, the rat was connected to the recording device and returned to the box, which was carried into the enclosure through one of three joins in the curtains, and placed in a pseudo-random location on the floor. On a different day, both lights were moved to a new location around the arena, so as to prevent the rat from forming a stable association with distant auditory 3 and olfactory cues that would interfere with landmark control. The sections were mounted and stained with Cresyl violet, and the slides were observed under a DM750 microscope (Leica, UK) in order to determine the site of the electrode track, which was verified using a rat brain atlas [24]

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