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Featured ArticleResearch Articles, Behavioral/Cognitive

Bilateral Discrimination of Tactile Patterns without Whisking in Freely Running Rats

Pauline Kerekes, Aurélie Daret, Daniel E. Shulz and Valérie Ego-Stengel
Journal of Neuroscience 9 August 2017, 37 (32) 7567-7579; https://doi.org/10.1523/JNEUROSCI.0528-17.2017
Pauline Kerekes
Unité de Neuroscience, Information et Complexité, Centre National de la Recherche Scientifique, FRE 3693, 91198 Gif-sur-Yvette, France
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Aurélie Daret
Unité de Neuroscience, Information et Complexité, Centre National de la Recherche Scientifique, FRE 3693, 91198 Gif-sur-Yvette, France
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Daniel E. Shulz
Unité de Neuroscience, Information et Complexité, Centre National de la Recherche Scientifique, FRE 3693, 91198 Gif-sur-Yvette, France
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Valérie Ego-Stengel
Unité de Neuroscience, Information et Complexité, Centre National de la Recherche Scientifique, FRE 3693, 91198 Gif-sur-Yvette, France
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    Figure 1.

    Behavioral maze and learning protocol for investigating whisker-based discrimination in the freely moving rat. A1, Schematic representation of the automated maze. For each trial, the rats had to run in the central alley through the main stimulus site (black rectangle, enlarged on the right). A smooth surface and a surface with a regular series of bars were displayed on the right and left sides randomly. At the end of the alley, the animals had to turn to the side on which the regular series of bars was presented to receive a reward. A2, After a period of habituation, task learning was divided into several stages. In stage 1, two reminders of the rewarded stimulus were displayed on the rewarded side: one at the end of the alley near the choice point (R1) and the other next to the reward site (R2). During stage 2, reminder R1 was displayed only. During stage 3, only stimuli at the main site were present. B, Top view of a rat running in the alley before contacting the stimuli. The blue rectangle encloses the tracking area. The corresponding enlargement shows tracking of the head direction using IR light reflection on the eyes (red lines) and tracking of the angle values of the right and left whiskers carrying reflection material (green lines). C, Variables measured during tracking. Top, Absolute angle of the right and left whiskers (respectively, θR and θL) relative to the head axis. When the whiskers are oriented toward the right side, θR < θL and the ratio is <1. Bottom, Head direction (γ) relative to the central alley (vertical on the video frames as in B).

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    Figure 2.

    Discrimination between a smooth surface and a surface with regularly spaced vertical bars in 8 weeks. A, Learning curves for stage 1 with two reminders of the rewarded stimulus. The animals had to achieve at least 80% of correct trials during three consecutive sessions to enter the following stage. B, Learning curves with one reminder at the choice position (same criterion as for stage 1). C, Learning curves for stage 3, with only the main stimuli present in the central alley. The criterion to complete learning was to maintain a mean performance of 70% with a maximal SD of 4.2% on 6 consecutive sessions. All curves have been aligned on the final session of learning for each rat (range 25–46 sessions). The inset details the performance within a session, calculated by splitting each session into 6 blocks of trials of equal length and averaged over the last 6 sessions of stage 3 (n = 6 rats). In this figure and the following, the thick dark line indicates the mean performance ± SEM and color traces show individual results.

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    Figure 3.

    Discrimination of surfaces with irregularly spaced bars from the smooth and regular stimuli. A, Profiles of the irregular series arranged by increasing width of the largest interval between bars. B, Replacement of either the regular or the smooth stimulus by the irregular I40 stimulus (n = 6 rats). In both panels, the pretest session (day before replacement) and the test session (day of replacement) are shown, split into six blocks of trials of equal length (20–28 trials depending on the animal). C, Performance divided by chance level after replacement of either the regular (square symbols) or the smooth (triangles) stimuli by each of the irregular series (I13, I30, I40, I48, and I50). The regular versus smooth performance in this figure was calculated as the mean performance during all pretest sessions.

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    Figure 4.

    Whisker cutting impairs discrimination. A, Performance for the session before and two sessions after whisker cutting (n = 7 rats). Each session (regular vs smooth) has been split into six blocks of trials. B, Performance averaged over all trials of the sessions before and after whisker cutting (n = 7 rats) and before and after anesthesia only (n = 3 rats). *p < 0.05, paired t-test.

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    Figure 5.

    Cortical inactivation impairs discrimination. A, Multiunit activity in response to stimulation of a functionally identified whisker as a function of time around the application of muscimol on the barrel cortex surface (n = 3 recordings in 2 rats). Inset, Peristimulus time histogram of the activity recorded on one tetrode while stimulating whisker D2 20 min before (black) and 60 min after (red) muscimol application. Activity 90 min after was null. B, Performance during a control session, during muscimol application, and during saline application (two rats) or no solution (one rat). Each session (regular vs smooth) has been split into six blocks of trials. C, Performance averaged over all trials of the sessions before and after muscimol or saline cortical application (n = 3 rats). *p < 0.05, paired t-test.

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    Figure 6.

    Discrimination of stimuli was performed without whisking. A, Left and right whisker angle as a function of time for an example discrimination trial in the central alley. B, Left and right whisker angle as a function of time during a spontaneous bout of whisking in a reward arm. C, Power spectrum of the whisker angle (n = 336 trials, 3 rats) and power spectrum of the traces of B showing a peak in the whisking frequency range.

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    Figure 7.

    Whisker angle and head direction during stimulus discrimination. A, Individual trial trajectories of the right whisker angle as a function of the rat position (measured as the eyes position) in the central alley for five regular versus smooth sessions in the same animal (n = 665 trials). The color indicates time within sessions (green: beginning; blue: end). Each point corresponds to the measure on one video frame; 27 frames were analyzed for each trial. Interval between two points was 10 ms. The thick black line indicates the mean trajectory. The red horizontal line indicates the physical position of the stimulus along the alley and the vertical arrow indicates the first possible contact between the whiskers and the stimulus if the whiskers were fully protracted. B, Mean (±SEM) right whisker angular trajectories for each of three rats as a function of the rat position in the central alley. The horizontal error bars represent the SD of the eye position distribution. For panels B–E, only successful trials were kept. C, Left (top) and right (bottom) whisker angle values as a function of the rat position in the central alley (n = 3 rats). In each panel, the angle values have been separated in two groups depending on whether the rewarded stimulus was on the right (black trace) or on the left (blue trace). D, E, Whisker angle ratio (right/left) and head direction plotted as a function of the rat position in the central alley (n = 3 rats). Angle ratios have been divided by their baseline value before averaging across animals.

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The Journal of Neuroscience: 37 (32)
Journal of Neuroscience
Vol. 37, Issue 32
9 Aug 2017
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Bilateral Discrimination of Tactile Patterns without Whisking in Freely Running Rats
Pauline Kerekes, Aurélie Daret, Daniel E. Shulz, Valérie Ego-Stengel
Journal of Neuroscience 9 August 2017, 37 (32) 7567-7579; DOI: 10.1523/JNEUROSCI.0528-17.2017

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Bilateral Discrimination of Tactile Patterns without Whisking in Freely Running Rats
Pauline Kerekes, Aurélie Daret, Daniel E. Shulz, Valérie Ego-Stengel
Journal of Neuroscience 9 August 2017, 37 (32) 7567-7579; DOI: 10.1523/JNEUROSCI.0528-17.2017
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Keywords

  • freely running behavior
  • somatosensory cortex
  • tactile discrimination
  • whiskers

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