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Generalization of Object Localization From Whiskers to Other Body Parts in Freely Moving Rats

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Generalization of Object Localization From Whiskers to Other Body Parts in Freely Moving Rats

David Deutsch et al. Front Integr Neurosci.

Abstract

Rats can be trained to associate relative spatial locations of objects with the spatial location of rewards. Here we ask whether rats can localize static silent objects with other body parts in the dark, and if so with what resolution. We addressed these questions in trained rats, whose interactions with the objects were tracked at high-resolution before and after whisker trimming. We found that rats can use other body parts, such as trunk and ears, to localize objects. Localization resolution with non-whisking body parts (henceforth, 'body') was poorer than that obtained with whiskers, even when left with a single whisker at each side. Part of the superiority of whiskers was obtained via the use of multiple contacts. Transfer from whisker to body localization occurred within one session, provided that body contacts with the objects occurred before whisker trimming, or in the next session otherwise. This transfer occurred whether temporal cues were used for discrimination or when discrimination was based on spatial cues alone. Rats' decision in each trial was based on the sensory cues acquired in that trial and on decisions and reward locations in previous trials. When sensory cues were acquired by body contacts, rat decisions relied more on the reward location in previous trials. Overall, the results suggest that rats can generalize the idea of relative object location across different body parts, while preferring to rely on whiskers-based localization, which occurs earlier and conveys higher resolution.

Keywords: active touch; decision; haptic; localization; sensory history; tactile; whisker.

Figures

FIGURE 1
FIGURE 1
Experimental setup and training procedure. Rats were trained to associate the spatial arrangement of two vertical poles with a reward side. (A) A rat from Group 1 (Narrow, Staircase; see Table 1) with a single whisker during task performance, top view. The reward (the sipper marked with V) was always given at the reference (posterior) pole side. In the Narrow configuration (Groups 1–2, see Table 1), the pole-sipper geometry was designed such that rats contacted the poles with their body on the way to the sippers. For all rats that were trained in the Narrow configuration, whiskers were trimmed gradually from a full pad to a single row (row C) to a single whisker (C2) to no whisker (Full-Row-Single-No). (B) The Wide configuration (Groups 3–4, see Table 1) was designed such that rats did not need to contact the poles with their body on the way to the sippers. In this configuration the distance between the poles is larger in the left-right axis, and the poles are closer to the sippers in the posterior anterior axis [compare (A) and (B); see section Materials and Methods for more details]. In Group 3, whiskers were trimmed from a full-pad to no-whisker (Full-No), while in Group 4 whiskers were trimmed gradually (Full-Row-Single-No). (C) Each rat was trained in one of two paradigms. In the Staircase paradigm (top; Groups 1, 3, 4) the offset in a given trial was chosen based on animal performance in previous trials. In the Block paradigm (bottom; Group 2) the offset in each trial was chosen randomly from three possible offsets in a given session, regardless of rat’s performance. The side of the reference pole (left or right) was chosen randomly (Block training) or pseudo-randomly (Staircase training) between trials (see section Materials and Methods). An example session is shown for each training paradigm. Hit trials are marked in blue, miss in red.
FIGURE 2
FIGURE 2
Localization by whiskers and body. (A) Distributions of localization thresholds in the single whisker (red) and no whisker (green) conditions (Group 1 - Narrow, Staircase). (B) Localization threshold (Te) for the two animals in Group 1. All-start/All-stable: sessions with all whiskers, start training (first sessions) and when behavior was stable (last sessions). Single/No – three sessions before/after trimming the last (bilateral) single whiskers. Te is defined as in Knutsen et al. (2006), see their Figure 10. Black lines indicate the median Te and the lower and upper end of the gray bars indicate the first and third quarantines, respectively. (C) Mean offset as a function of trial number for two animals. Means over the last 5 sessions with a single whisker (red), the first session after trimming (black) and the mean over sessions 2–5 after trimming (green). Black dotted line and gray shade are the mean and standard deviation for the offset of a rat performing at chance level (N = 5000 simulated sessions).
FIGURE 3
FIGURE 3
The use of whiskers and learning. (A) In the Narrow configuration, Block training paradigm (Group 2), performance is shown for large offsets (≥14 mm) and small offsets (≤10 mm). Black line – mean over all trials in the last 3 sessions before/after trimming (labeled in red/green as single/no whisker). Each symbol represents the rate of success of an individual rat. (B) Time from the Decision (turning) Point (see Results) to first contact between the body and any pole. Positive time means that the first body-pole contact occurred after the rat started the final turning. Group 3, full pad, Wide configuration, Staircase paradigm. (C) Two last sessions per rat before trimming (red), and first session after trimming (black) are shown for the three rats in Group 3. Dots represent the minimum offset in the session, after running a 10-trial moving average. Performance at chance level is shown as in Figure 2C. (D) Change in performance around trimming (comparing three sessions before/after trimming) for rats in Group 2 (Narrow, Block). Each symbol represents the percent of change in performance for an individual rat (comparing mean performance before and after trimming; negative value means drop in performance). Performance dropped for all six rats when trimmed from full-pad to a single row (‘All to Row’), and for 5/6 rats when trimming from a single row to a single whisker (‘Row to Single’). (E) Each line connects the mean localization thresholds over three sessions before and after each trimming step, for each rat.
FIGURE 4
FIGURE 4
Decision points. (A) The mean and standard error of the head trajectories in left choice (blue) and right choice (red) trials for the rats in Group 2 (Narrow geometry, Block training). Data from the 3 sessions before trimming the single whisker. Solid arrow marks the last point where the left and right trajectories diverged. Red arrow marks the first point in which the difference between the two trajectories was larger than twice the sum of the standard errors from both trajectories. (B) Same as (A), but for the 3 sessions after trimming the single whisker. (C,D) same as (A,B), but at the Narrow/Staircase configuration. (E) A single session example from a control session. In control sessions the poles were removed from the setup. The pole base was still moving with the same logic (controlling for sound-based discrimination). Animal performance dropped to chance, with typically long epochs of repeated choice (here, a right-choice sequence is seen), showing that rats rely on tactile rather than auditory cue in the task. (F) Left/right head trajectories in the no-pole condition.
FIGURE 5
FIGURE 5
Temporal and spatial coding.(A) Mean performance for the Block-trained (Group 2, blue; Narrow geometry) and Staircase-trained (Group 1, red; Narrow geometry) rats, for small offsets (offset ≤ 10 mm for Block-trained, offset < median for Staircase-trained) and for large offsets (dotted line; offset ≥ 14 mm for Block-trained, offset > median for Staircase trained) rats. Performance is shown separately for trials with DTp-a < 0 (left) and for trials with DTp-a > 0 (right). (B) Mean performance for positive DTp-a (purple) and negative DTp-a (green), as a function of pole offset. (C) The fraction of trials with multiple (>1) whisker contacts with the reference pole. (D) Mean protraction amplitude in the whisker contacting the reference pole, as a function of offset. (E) Mean performance in trials where whiskers touched both poles (black), only the reference pole (dark gray) or only the anterior pole (light gray). (F) Further training in fixed offset. Top, illustration of poles arrangements: ‘original’ (middle, reference pole at the same location as during early training), ‘proximal’ (closer to entrance to the task area) and ‘distal.’ Arrow indicates the entrance-line to sipper-line direction. Each line represents the mean success rate of a rat during the first two sessions after moving to the changing-reference paradigm. Squares indicate the mean success rate of each rat in the last two sessions before moving to the non-fixed reference paradigm. (G) Curving index (CI, see section Materials and Methods) distribution. (H) Rat performance versus CI; mean over 6 rats and 581 trials. (I) Head trajectory (mean and standard error) for hit (left) and miss (right) trials.
FIGURE 6
FIGURE 6
Dependence of decisions on previous trials. (A) Mean performance as a function of offset for six rats (Group 2 - Narrow, Block) given hit (blue) or miss (red) in the previous trial. Black asterisk indicate significant difference between hit/miss trials for a given offset after Bonferroni correction for multiple comparisons. (B) Probability for repeating the same choice as in the previous trial (left after left or right after right), given hit (blue) or miss (red) in the previous trial. Red asterisk indicates significance before but not after correction for multiple comparisons. (C,D) Same as (A,B), but for the three rats in Group 4 (Wide, Staircase).

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