Whisker movements reveal spatial attention: a unified computational model of active sensing control in the rat

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.

Figure 1. Rat behaviour.

(Top) Three still frames from a top-down video recording of a rat encountering and orienting to the corner of a square object with vertical walls (data from [20]). Each successive frame is at approximately the time of maximum protraction of three consecutive ‘whisks’ (t = 0 ms, 120 ms, 230 ms)—the first is that immediately following the rat's first contact with the object. Two behavioural responses can be seen in the subsequent frames: (i) the whiskers are positioned asymmetrically around the snout and (ii) the tip of the snout is brought to the point of contact with the object. The whole video (covering the same time range as the plot) is available as Video S1. (Bottom) Average bilateral protraction angle of the whiskers recovered from the same video over a time period covering the encounter (left/right is black/grey; vertical scale bar has length 30°). Main feature of these signals until contact at t = 0 ms is periodic protraction and retraction known as ‘whisking’. The times of the three still frames are marked as dots on the trace from the left hand whiskers (see main text).

Figure 2. Model.

Solid arrows indicate causal influences. Multiple influences affect the attended spatial region. One key influence will be whisker-environment contact (‘tactile signal’); others will include data from other sensory modalities and endogenous influences (‘other signals’). The ‘attended region’ drives both ‘whisker movement’ (rapidly and consistently) and ‘head movement’ (on a longer timescale, and only when this is not precluded by local geometry). Dotted lines show relationships that have been observed in animals. CIA is a correlation between contact and asymmetry in whisker movement. HTA is a correlation between turning of the head and asymmetry in whisker movement.

Figure 3. Implementation of the model.

Boxes indicate components, solid arrows indicate causal influences. Extends/modifies model of Figure 2 with implementation-specific components: attended region made explicit as salience map(s); ‘other signals’ implemented as an endogenous stochastic source; inhibition, including a contribution from inhibition-of-return (IOR) system; oscillator (OSC); ‘physical plane model’ simulates mechanics. Separate salience channels are maintained for tactile and ‘other’ signals and selected at switch (SW). Data snapshot. Within the boxes is displayed a data snapshot from a point of maximum protraction during a whisk against a vertical surface. Physical plane model in world-centric coordinates includes head, whiskers and obstacle surfaces; whisker contacts are shown as dots (darker dots indicate stronger bending) and current target of foveation as a ‘target’ icon. Tactile and ‘other’ signals are mapped into head-centric excitation maps which drive salience maps (darker areas represent higher salience; pattern corresponding to wall can be seen in tactile salience map). Activity in salience map regions inside obstacles as well as in previously-visited regions (IOR, see text) is inhibited. Tactile salience channel is selected at SW owing to higher peak salience than ‘other’ channel. Whisker movement panel shows maximum protraction computed to roughly achieve MIMC with respect to attended region. Head movement panel shows current target of foveation (target icon) at peak of salience map. Video S4 shows the operation of the implementation during a trial including this snapshot (which was taken at t = 0.340).

Figure 4. Plane model detail.

Head (light grey) location/orientation is defined by and . Nearby obstacle (dark grey). Whisker base is located on ‘mystacial pad arc’ (dashed curve) which traces the snout outline (open dot marks arc center). Whisker shaft angle at the base, denoted , is defined with respect to head midline (dotted lines). Unperturbed whisker arc (upper solid line) intersects obstacle. Perturbed whisker arc (lower solid line) is found by adjusting curvature caudally until no intersection occurs. Deviation of point marked with solid dot from unperturbed to perturbed arc is denoted .

Figure 5. Whisking pattern generation.

(Lower trace, axis to right) Solid line marked at each sample with dots is whisking drive signal, . (Upper traces, axis to left) Thin dotted and solid lines indicate maximum retraction and protraction angles ( and ), respectively, for one whisker (the most rostral whisker on the left). Overlaid thick lines show the target protraction angle, , which is equal to or depending on the value of (see Equation 9). Feint vertical lines show the time of oscillator ticks (times of falling edges in ). Actual whisker protraction angle, , is indicated by the dashed line and is driven towards . A sharp increase in maximum protraction angle occurs shortly before 0.5 s; this change is reflected in the whisker protraction angle most strongly during the subsequent protraction which ends at around 0.6 s.

Figure 6. Head-turning asymmetry.

(A) Results from model. Each dot represents one sample; solid line is line of best fit. Also shown are lines of best fit from analogous observations made by Towal & Hartmann (2006) (dotted line, their Figure 6a) and Mitchinson et al. (2011) (dashed line, their Figure 4a(i)). Note, therefore, that results from simulated model fall between results from two behavioural studies. (B) Results from Towal's & Hartmann's behavioural experiment , reproduced with permission. (C/D) Stills from model (C) and behavioural experiment (D) showing asymmetry in bilateral protraction angles during head turn to the right. Still in (C) is taken from Video S5.

Figure 7. Contact-induced asymmetry.

(A) Results from model (see text for analysis method). Mean protraction angle of the whiskers on the left (or right—see text) in NEAR relative to mean value in FAR, plotted against the binned location, , relative to the fovea of a single nearby wall (4 mm square bins). Red/white/blue indicates mean protraction angle is reduced/equal/increased relative to , with full saturation for each colour indicating difference. White semi-circle indicates 25 mm from fovea at , i.e. the region graphed in Figure 4c of Mitchinson et al. (2007) . (B) Results from behavioural experiment (in rat, , their Figure 4c), re-analysed on a rectangular grid to match current analysis. Electromyogram strength in NEAR, rather than mean protraction angle, is graphed, relative to mean electromyogram strength in FAR; fully saturated red/blue indicates 33% difference. (C/D) Stills from model (C) and behavioural experiment (D) showing asymmetry in bilateral protraction angles driven by encounter with angled surface. Still in (C) is taken from Video S6.

Figure 8. Spread-reduction.

(A) Results from model. Solid/dotted/chained lines are maximum/mean/minimum spread within the whisk, against whisk type (see text). (B) Results from behavioural experiment (in rat, , their Figure 2b), data re-plotted. (C/D) Stills from model (C) and behavioural experiment (D) showing the trial condition of rat approaching vertical obstacle (three panels in each case show time of maximum protraction in pre-contact, first and second contact whisks). Stills in (C) are taken from Video S7.