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Sunday, 4 December 2016

Whisker Movements Reveal Spatial Attention: A Unified Computational Model of Active Sensing Control in the Rat

. 2013 Sep; 9(9): e1003236.
Published online 2013 Sep 26. doi:  10.1371/journal.pcbi.1003236
PMCID: PMC3784505


Gunnar Blohm, Editor
1Department Of Psychology, The University Of Sheffield, Sheffield, United Kingdom
Queen's University, Canada
The authors have declared that no competing interests exist.
Conceived and designed the experiments: BM TJP. Performed the experiments: BM. Analyzed the data: BM. Wrote the paper: BM TJP.

Abstract

Spatial attention is most often investigated in the visual modality through measurement of eye movements, with primates, including humans, a widely-studied model. Its study in laboratory rodents, such as mice and rats, requires different techniques, owing to the lack of a visual fovea and the particular ethological relevance of orienting movements of the snout and the whiskers in these animals. In recent years, several reliable relationships have been observed between environmental and behavioural variables and movements of the whiskers, but the function of these responses, as well as how they integrate, remains unclear. Here, we propose a unifying abstract model of whisker movement control that has as its key variable the region of space that is the animal's current focus of attention, and demonstrate, using computer-simulated behavioral experiments, that the model is consistent with a broad range of experimental observations. A core hypothesis is that the rat explicitly decodes the location in space of whisker contacts and that this representation is used to regulate whisker drive signals. This proposition stands in contrast to earlier proposals that the modulation of whisker movement during exploration is mediated primarily by reflex loops. We go on to argue that the superior colliculus is a candidate neural substrate for the siting of a head-centred map guiding whisker movement, in analogy to current models of visual attention. The proposed model has the potential to offer a more complete understanding of whisker control as well as to highlight the potential of the rodent and its whiskers as a tool for the study of mammalian attention.

Author Summary

The management of attention is central to animal behaviour and a central theme of study in both neuroscience and psychology. Attention is usually studied in the visual system (most often using cats or primates) owing to the ease of generating controlled visual stimuli and of measuring its expression through eye movement. In this study, we develop a model of the expression of attention in another sensory modality, that served by the tactile whiskers of small mammals (such as rats and mice). This sensory system has long been a popular model in neuroscience and is well characterised. It has become recognised in recent years that the modulations of whisker movements prevalent in the behaving animal represent “active sensing” (in the sense of moving the sensors to optimise sensing performance), yet a unified understanding of these modulations is still lacking. Our model proposes just such a unified understanding, suggesting that whisker movement modulations can be understood as an overt expression of the animal's changing focus of attention. This proposal, therefore, offers to provide both an enhanced understanding of the whisker sensory system and an insight into the management of attention in these animals.