Tactile Attention in the Vibrissal System
|Ben Mitchinson (2015), Scholarpedia, 10(3):32361.||doi:10.4249/scholarpedia.32361||revision #150524 [link to/cite this article]|
Attention is a rich research area concerning itself with many aspects of brain function and animal behaviour (even as far as consciousness). This article focuses on the most prosaic aspect of attention, however, that of overt orienting of sensory receptors to the location of an 'attended stimulus' in space. Whilst overt orienting of the eyes has been studied in great detail, orienting of the vibrissal array of rodents has only recently begun to be investigated, despite the importance of this organ as an experimental model to a wide variety of investigations. This article reviews current understanding of orienting in this organ and identifies major open questions.
The expression of attention
Attention as a faculty of neural systems need not, in general, have a direct behavioural correlate (or, in principle, any behavioural correlate at all). Purported system variables associated with 'covert' attention management can be measured behaviourally only indirectly through the impact they have on subsequent stimulus-response or object search times or efficiencies (Ward 2008). Models of attentional mechanisms can be complex and multi-faceted in attempting to account for the effects of immediate sensory stimuli, prior knowledge, motivation, instruction, and so on, on the variables visible through these relatively small apertures (Frintrop et al. 2010). These models have been developed using data from visual system studies (in models such as cat and primate); attention is often studied using human participants since the required manipulations are often not invasive (Posner 1980).
Despite the complexity of the evolution of these internal states, however, the 'overt' orienting of the sensory organs, the head, and the body, to focus sensory apparatus onto a selected region of space (the 'orienting reflex') is both a rather more straightforward expression of attention switching and absolutely central to everyday behaviour (Itti and Koch 2001). In primates, orienting is typically led by the visual system's fovea and is modelled as a series of discrete 'saccades' of the visual fixation point from one spatial location to the next (Itti et al. 1998). This behaviour is predictable, and has been characterised in a range of tasks including, for instance, scene search (Yarbus 1967), reading (Rayner 1998) and locomotion (Hollands et al. 1995). The contemporary ease of measuring eye movements in a human subject facilitates the use of this model (Duchowski 2007).
Rodent models of attention
Whilst observation of primate visual systems provides relatively controlled access to attentional mechanisms, and particularly to spatial variables, the use of rodent models may be desirable for some studies, for example if the goal is drug discovery or if the manipulation is otherwise invasive. Techniques for observing attentional mechanisms in rodents are less comprehensive, but a variety of choice/reward protocols have been employed which make use of the spatial component of the apparatus only for the indication of the choice (Sagvolden et al. 2005). One well-established paradigm is the 5-choice serial reaction time task (5CSRTT) (Robbins 2002) which comprises the measurement of the procedure and timing of nose-poking into apertures signalled by (paradigmatically, visual) stimuli. Results from the 5CSRTT are described as indicating characteristics such as 'impulsivity' and 'compulsivity' (Robbins 2002, Sanchez-Roige et al. 2012). The potential relevance of this paradigm to research into contemporary medical problems such as attention-deficit disorders is clear (in fact, the task was originally designed with just such investigations in mind).
The sensory modality upon which rodents rely the most is, under many conditions, the tactile whisker (vibrissa) system rather than vision (see Vibrissal behavior and function). One consequence of that in this context follows from the observation that 'orienting' of the tactile whisker sensory organ to a spatial location implies the bringing of the organ to, rather than just the pointing of the organ towards, the target of attention, a result of the fundamentally limited range of tactile sensing (Mitchinson and Prescott 2013). Thus, the animal's morphology dictates a convergence between sensory orienting and 'taking action' (which might include, for example, the orienting of motor resources such as the mouth and locomotion to a location from where action can be taken). Investigations using Whiskered robots have demonstrated that linking a changing focus of spatial attention to orienting of the snout generates plausible sequences of gross behaviour (Mitchinson et al. 2012, Mitchinson and Prescott 2013, Prescott et al. in press). This convergence has previously been described using the expression orienting is acting (Mitchinson in press). Note that this convergence is present in all systems to an extent even though it is much less marked when it is remote sensors that are being oriented.
Meanwhile, whilst many animals can move their eyes within their heads, so many whiskered animals—certainly, rodents—appear able to reposition their whiskers about their heads (Sofroniew and Svoboda 2015). Most models to date of the control of these movements have been based fairly directly on measured relationships between whisker movements and immediate sensory and motor variables rather than on central mechanisms (Towal and Hartmann 2006, Mitchinson et al. 2007, Grant et al. 2009, Deutsch et al. 2012, Arkley et al. 2014), but an analogy between these movements and saccadic movements of the eyes (which are defined in physical space) has been drawn more than once (Towal and Hartmann 2006, Pearson et al. 2007, Mitchinson et al. 2014, Sofroniew and Svoboda 2015). Taken together, these observations suggest an identification between the control of the whiskers and snout and the control of the eyes and head, both driven by the animal's changing focus of spatial attention.
A model of spatial attention mediated by vibrissae
This identification is supported, also, by the nature of observed whisker movements, and one model of whisker movement control has been proposed that makes this identification explicit, having at its core a state representing the region of space attended by the animal (Mitchinson and Prescott 2013). The model provides a succinct explanation for several observations of whisker movement and makes predictions as to how direct manipulation of the animal's spatial attention will be reflected through those movements. Experimental implementation of the model expresses rodent-like exploratory behaviour as a 'series of orients' analogous to the 'series of saccades' model of visual orienting behaviour, underlining both this analogous relationship and also the connection in the case of the rodent model with gross behaviour.
Description of the model
In brief, the model dictates that whiskers will be moved so as to bring them to bear on attended objects. Thus, its central variable is a representation of the immediate region of space attended by an animal, which we can refer to as the locus of spatial attention or the 'attended region' (Figure 1). This region may be compact or extensive, though 'objects' are not explicitly delineated (a distinction is usually drawn between location-based and object-based attention).
Behavioural studies have indicated that the movement of all of the whiskers on each side of the face can be well-summarised by only two variables (Grant et al. 2009); however, such a summary does not account for the shaping of the 2D surface formed by the whisker tips (Huet and Hartmann 2014). Accordingly, a fixed transform, which may be arbitrarily non-linear, maps from the representation of the attended region to the maximum protraction angle of each of the whiskers individually. This transform is chosen so that each whisker tends to be driven forward into the attended region by a small amount. A separate model component generates the rhythmic 'whisking' motion characteristic of this system (see Whisking kinematics and Whisking pattern generation) so that the instantaneous protraction angle of each whisker is derived by combining the outputs of these two systems, and whiskers are palpated in and out of the attended region.
Meanwhile, the movement of the snout of the animal (specifically, the positioning of a generalised sensory ‘fovea’ around the mouth) is driven by the same representation on a longer timescale. In this model, whisker and head movements are both, therefore, generated as overt expressions of this attended region. Interactions between the animal and its environment then modulate the locus of spatial attention through the sensory systems; in particular, contacts between the whiskers and objects in the environment excite attention directly.
The model has been used to simulate a range of behavioural experimental paradigms and has generated results in each case that are qualitatively and quantitatively similar to those reported in animals. First, 'Head-Turning Asymmetry' (HTA) is a relationship that has been observed in rat, mouse, and opossum (Towal and Hartmann 2006, Mitchinson et al. 2011). Turning of the head is preceded by asymmetry in the protraction angles of the whiskers on each side of the head such that the whiskers appear to 'lead' the head movement. Second, 'Contact-Induced Asymmetry' (CIA, Figure 2) is a relationship between whisker-environment contact and protraction angle asymmetry (Mitchinson et al. 2007, Mitchinson et al. 2011, Deutsch et al. 2012). Contact with the environment on one side only leads to less/more protraction on the ipsilateral/contralateral side. Third, 'spread reduction' (SR) denotes the finding that the spread between the protraction angles of whiskers on each side is reduced during environmental contact (Grant et al. 2009, Huet and Hartmann 2014).
Each of the observations listed can be alternatively interpreted as indicating a single direct reactive mechanism. However, the model based on spatial attention is sufficient to produce all of them from a single, albeit more complex, mechanism. Moreover, the attention-based model can explain anticipatory modulations of whisker movement, which reactive mechanisms cannot, and there are now many observations of these (Sachdev et al. 2003, Berg and Kleinfeld 2003, Mitchinson et al. 2007, Grant et al. 2009, Arkley et al. 2014, Voigts et al. 2015).
Direct manipulation of the animal's attention will be required to make a direct test of the model, and this experiment has not yet been performed. Given the potential for confound with direct influences on whisker movement, manipulating attention using a non-tactile modality may be the preferred experimental approach (audio or olfactory stimuli might be suitable, for instance).
Methodologically, the measurement of whisker motions has become far easier over recent years primarily owing to the increased availability of high-speed and high-sensitivity videography (Diamond and Arabzadeh 2013) (coincidentally, eye movement tracking has become more accessible over much the same period, though for different reasons). As a result, measurement of whisker motion has become a potentially-useful general tool for accessing the animal's state, apart from its use in the analysis of whisker operation per se (for instance, see (Wolfe et al. 2011)). Whilst whisker motions can now be measured even in freely-behaving preparations (Arkley et al. 2014), they are available in the head-fixed preparation also (which would stand in the way of choice protocols such as 5CSRTT), and measurement can be largely automated in both cases (see Clack et al. 2012 and references therein).
Potentially, then, whisker motion measurement provides a window onto attentional mechanisms in conditions that are highly flexible and amenable to direct neural measurements and interventions. The establishment of direct connections between whisker movements and hidden attentional state variables would offer a powerful new tool for the study of attention in a rat model. Such a tool would provide access to states not available through established paradigms such as the 5CSRTT and, since whisker movements are known to respond to sensory events on very short timescales (10-15 ms, Mitchinson et al. 2007), with good temporal as well as spatial resolution. The degree to which vibrissal attention would share mechanisms and resources in rodents with other modalities would be an open question, but cross-modal effects on attention are very well established, at least, in humans (Driver and Spence 1998).
If a connection between attention and whisker movement can be validated, it will have two impacts. First, as discussed, by providing a minimally-invasive tool for accessing attentional states in the behaving animal. Second, by providing a more complete understanding of how the whiskers are used by the animal to serve the purpose of Active tactile perception. Through the relationship with gross behaviour, it is perhaps particularly clear in animals that rely so heavily on their whiskers how closely these two concepts—attention and active sensing—are linked.
Given the importance of this system to many areas of neuroscience, a complete understanding of how the whiskers are moved in response to exogenous and endogenous influences would be very valuable. Indeed, experimental paradigms whereby whisker stimulation occurs as a result of whisker movement, rather than of stimulator movement, are necessary if the decoding of sensory signals is to be understood (see Vibrissal location coding).
Any commonalities identified between these two popular models (visual and vibrissal) would, per se, be a great step forward in terms of synthesis. Lines of enquiry in this regard could include investigations of whisker sensory and motor characteristics of brain areas involved in the management of spatial attention and the generation of spatially-targeted behaviours including visual orienting. An obvious example is superior colliculus, which is a well-studied area in general (May 2006, Gandhi and Katnani 2011) and has generated a slew of promising results in studies of the vibrissae both historically and more recently (see Bezdudnaya and Castro-Alamancos 2014 for a recent contribution, also see references in Mitchinson and Prescott 2013).
Intriguingly, though, it may be the differences between these systems that has the potential to be most revealing (Mitchinson and Prescott 2013). There is both neurophysiological (Benedetti 1991) and morphological (Huet and Hartmann 2014) evidence that whisker sensory signals are brought into register with visual signals in rat colliculus, a result which is itself unsurprising (Stein and Stanford 2008). Bringing into register sensory signals from modalities with mobile sensory organs requires dynamic remapping, however. In the case of the whiskers, which constantly move back and forth through space during active sensing, this remapping must occur at multiple cycles each second, a fact which may help to highlight the underlying mechanism. Meanwhile, orienting of the eyes—a remote sensor—requires the control only of azimuth and elevation, and representations of space in colliculus are exclusively described as being two-dimensional (Itti and Koch 2001) (very likely, it seems, correspondingly). In contrast, the control of just the snout (let alone the whiskers) requires a richer representation of space; on the face of it, all three dimensions must be represented, since the snout must be directed to not just towards the target of attention (Mitchinson and Prescott 2013). Understanding how these two systems, primate and rodent, correspond in these regards is bound, it seems, to be instructive.
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