PLoS Comput Biol. 2013 Sep; 9(9): e1003236.
Published online 2013 Sep 26. doi: 10.1371/journal.pcbi.1003236
PMCID: PMC3784505
Gunnar Blohm, Editor
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.