Proposed Scheme of Afferent Conduction of Active-Touch Signals

<p>Whisking signals (W) are conveyed by the paralemniscal pathway (para) via the POm and are proposed to involve whisking control. Touch signals (T) are conveyed by the extralemniscal pathway (extra) via VPMvl, and are proposed to involve processing of object location (“where”). Combined whisking–touch signals (WT) are conveyed by the lemniscal pathway via VPMdm, and are proposed to involve processing of object identity (“what”).</p

Distributions of Normalized Touch Responses in the Thalamus

<p>(A) TI value of each of the recorded neurons is indicated by a color code on its relative location in the canonical thalamic map defined in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.0040124#pbio-0040124-g001" target="_blank">Figure 1</a>D. (B) Distribution of TI in VPMdm ( <i>n</i> = 30), VPMvl ( <i>n</i> = 13), and POm ( <i>n</i> = 24). </p

Distributions of Thalamic Latencies and Durations According to Response Type

<div><p>(A) Latencies from protraction onset to half-peak response of all thalamic neurons during touch trials.</p> <p>(B) Latencies from relevant stimulus (contact time for Touch neurons and protraction onset for the rest) to half-peak response of all thalamic neurons during touch trials.</p> <p>(C) Response durations of individual cells during touch trials, measured from the PSTH, as the period during protraction in which the response was above 0.1 of its maximum.</p></div

Whisking and head motion in freely moving rats.

<p>Examples of whisker trajectories (filtered at 80 Hz) from freely-moving rats performing a localization task <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044272#pone.0044272-Knutsen1" target="_blank">[6]</a>, demonstrating the occurrence of whisks with a single peak (gray) and multiple peaks (red) after contact onset.</p

Fast Feedback in Active Sensing: Touch-Induced Changes to Whisker-Object Interaction

<div><p>Whisking mediated touch is an active sense whereby whisker movements are modulated by sensory input and behavioral context. Here we studied the effects of touching an object on whisking in head-fixed rats. Simultaneous movements of whiskers C1, C2, and D1 were tracked bilaterally and their movements compared. During free-air whisking, whisker protractions were typically characterized by a single acceleration-deceleration event, whisking amplitude and velocity were correlated, and whisk duration correlated with neither amplitude nor velocity. Upon contact with an object, a second acceleration-deceleration event occurred in about 25% of whisk cycles, involving both contacting (C2) and non-contacting (C1, D1) whiskers ipsilateral to the object. In these cases, the rostral whisker (C2) remained in contact with the object throughout the double-peak phase, which effectively prolonged the duration of C2 contact. These “touch-induced pumps” (TIPs) were detected, on average, 17.9 ms after contact. On a slower time scale, starting at the cycle following first touch, contralateral amplitude increased while ipsilateral amplitude decreased. Our results demonstrate that sensory-induced motor modulations occur at various timescales, and directly affect object palpation.</p> </div

Fast, within-cycle touch-induced ipsilateral feedback.

<p><b>A.</b> Angle trajectory from a contact trial, filtered at 80 Hz. Whisker C2 (red) touched the pole near the end of protraction. Touch events are indicated by black horizontal lines. TIPs (manually detected in this example) are indicated by asterisks. The first touch depicted was also the first touch in the trial. Data for ipsilateral C2 (red), ipsilateral C1 (black), and contralateral C2 (blue) whiskers. <b>B.</b> Angle trajectory of whisks with TIP (red) and without (grey), all taken from a single trial. Time and angle are presented with respect to their values at touch onset. <b>C.</b> Example of a touch-induced pump (TIP) that, after contact between whisker C2 and the pole, occurred simultaneously in the three untrimmed whiskers (C1, C2, D1). The C2 whisker was continuously in contact with the pole throughout the period marked touch (bold red line), so the whisker palpates against the pole without detaching from it. The TIP peak or onset (indicated by the arrow), the time of the first peak after touch, is followed by negative velocity. <b>D.</b> Time from touch onset (start of red bold line in C) to TIP onset (arrow in C) in contact trials (purple). The average latency of touch-induced pumps was 17.9 ms. The distribution of times between pseudo-touches (crossing of a threshold angle in free-air trials) and pump onset was normalized to have the same number of touches as in the contact data and is denoted in green. <b>E.</b> Inter-pump-interval (time between touch onsets in two neighboring whisks-with-TIP) with experimental (purple) and simulated (control; green) data. The control distribution is what is expected if the pumps had the same probability to occur, but were distributed randomly upon touch events. The peak around 140 ms is due to pumps that occurred in successive whisks (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044272#s2" target="_blank">Materials and Methods</a> for detailed description on the controls used in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044272#pone-0044272-g003" target="_blank">Figs. 3D and 3E</a>).</p

Whisking kinematics in free-air and after contact.

<p><b>A.</b> Distribution of whisk duration in free-air (dark green) and in contact (light green) trials. <b>B.</b> Distribution of whisk amplitudes in free-air (dark blue) and contact (light blue) trials. The distributions in A and B where smoothed using the MATLAB function <i>fitdist</i> (‘kernel’, width = 2). <b>C.</b> Correlations between the amplitude and duration of pairs of whisks, as a function of the interval between them. <b>D.</b> Whisk duration, amplitude, and set point, before the first “pseudo touch” (free-air trials; green) and the first (real) touch (contact trials; red for the ipsilateral and blue for contralateral sides).</p

TIPs occur more often in whisk cycles with higher set-points.

<p><b>A.</b> The average angle trace of whisker C1 (not touching) triggered on the onset of touch by whisker C2 for all whisks with (purple; mean ± SE) and without pumps (grey; mean ± SE). <b>B.</b> Similar to A, but when only data from the first touches in a trial (N = 140) were used. <b>C.</b> Mean trace around touch with TIP (purple) and over a subset of traces around touch with no TIP (control; green) for the data in A. The control subset was chosen by removing traces with the lowest set points, so that the mean set points of the control (green) and pump (purple) traces will be equal. <b>D.</b> Similar to C, but when only data from the first touch occurring in a trial was used.</p

Contact durations are longer in whisks with TIP.

<p><b>A.</b> A typical single whisk with a pump after touch onset. Period of whisker-pole contact marked in black. The pump occurred while the whisker stayed in contact with the pole. <b>B.</b> A typical single whisk without a pump after touch onset. <b>C.</b> Touch duration as a function of the position of the touch in a sequence of touches. Whisks with touch and TIP (purple) and whisks with touch but no TIP (gray). <b>D.</b> Touch duration with and without a TIP, as a function of the set point.</p

Whisking amplitudes, durations, and set-points after first touch.

<p><b>A.</b> Whisking angle of the ipsilateral C1 whisker (red) and contralateral C1 whisker (blue). Onset of the first touch in a trial is marked by a vertical line. <b>B.</b> Protraction amplitudes of whisker C1 as a function of whisk cycle, around first touch (red, blue) or first pseudo touch (dotted red, dotted blue). Ipsilateral C1 whisker (red, dotted red) and contralateral C1 whisker (blue, dotted blue). The most rostral untrimmed whisker C2 is touching the pole (the rare trials where whisker C1 also touched the pole in any of the first contacts were excluded from this analysis). Whisk cycle 0 is the first whisk with touch (or pseudo touch) in the trial. Asterisks indicate significant difference between ipsi and contralateral sides. We note that since the number of pseudo-touches was smaller than the number of real contacts, the error bars in the pseudo-touch trials were usually larger. <b>C.</b> Set point around touch as a function of whisk cycle. <b>D.</b> Same as B, but for retraction amplitude (negative value indicates retraction). <b>E.</b> Whisk duration around first touch. <b>F.</b> Probability of time-lags for contact and free-air trials.</p