To attribute spatial meaning to sensory information, the state of the sensory organ must be represented in the nervous system. In the rodent's vibrissal system, the whisking-cycle phase has been identified as a key coordinate, and phase-based representation of touch has been reported in the somatosensory cortex. Where and how phase is extracted in the ascending afferent pathways remains unknown. Using a closed-loop interface in anesthetized rats, we found that whisking phase is already encoded in a frequency- and amplitude-invariant manner by primary vibrissal afferents. We found that, for naturally constrained whisking dynamics, such invariant phase coding could be obtained by tuning each receptor to a restricted kinematic subspace. Invariant phase coding was preserved in the brainstem, where paralemniscal neurons filtered out the slowly evolving offset, whereas lemniscal neurons preserved it. These results demonstrate accurate, perceptually relevant, mechanically based processing at the sensor level.
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We thank D. Kleinfeld, N. Ulanovsky and A. Finkelstein for discussions. This research was supported by the Israel Science Foundation (grant no. 1127/14), the Minerva Foundation funded by the Federal German Ministry for Education and Research, the United States-Israel Binational Science Foundation (BSF, grant no. 2011432), the NSF-BSF Brain Research EAGER program (grant no. 2014906) and a fund from Lord Alliance for Life Science Collaboration. E.A. holds the Helen Diller Family Professorial Chair of Neurobiology.
The authors declare no competing financial interests.
Integrated supplementary information
(a) Controller scheme. The controller has a two components architecture: (i) a feedforward Inverse Model (IM) which maps the desired local trajectory ( and ) to a motor command . This model was realized by an artificial neural network (with one hidden layer of 3 logistic neurons and a single linear output neuron) trained iteratively at the beginning of each experiment. (ii) a feedback Proportional-Integral-Derivative (PID) controller which uses the error en = - θn-1 to produce a motor correction signal . This signal is required to compensate for inverse model inaccuracy and to track changes in the controlled motor plant, i.e., the whisker pad complex. Note that since stimulation rate is 83Hz and whisker tracking rate is 500Hz, each value of θ * and θ is in fact a vector of 6 numbers. (b) The dynamics of the PID output during synthetic whisking in two different rats. The protocol consisted of 7s long whisking bouts (shaded areas) separated by 5s rest periods. Changes in PID output reflect the dynamics of the motor plant, likely due to muscle fatigue. (c) Short-term dynamics of the change in PID output (mean±std of the last 10 bouts of synthetic whisking portrayed in panel b). In one rat the output transiently increased (purple), signifying muscle ‘depression’, while in the other the output decreased (blue), signifying muscle ‘potentiation’. (d) Long-term dynamics of the PID output (mean±std within each bout in panel b). One rat exhibited drastic potentiation (expressed in a decrease in PID output, purple) followed by long-term stability, while the other exhibited slowly evolving depression (blue). These different behaviors, both in the short- and long- term, probably reflect different ratios of protracting/retracting muscles stimulated in each experiment. The advantage of the PID controller is that it can track these multiple-timescale processes without the need to model them.
(a) Distribution of whisking amplitudes tested (0≤ θ amp ≤18). (b) Distribution of whisking offsets (relative to resting position) tested (0≤ θ off ≤35). (c) Distribution of whisking frequencies tested (4≤f≤10). (d), Distribution of the ratio between protraction and retraction durations. (e), Normalized autocorrelation functions of the four variables in panels a-d. Note that while the amplitude and offset were gradually changed between cycles, both whisking frequency and protraction-retraction ratio were randomized for each cycle independently (hence their autocorrelation drops steeply within the duration of a single cycle).
(a) Example of an LNP model constructed for a TG unit. The whisker trajectory recorded in-vivo is fed into the causal MID filter of the neuron. The output of this filter (i.e., the MID projection of the whisker kinematics) is then transformed into rate using the non-linear conditional probability distribution of the neuron, p(r|θ∙MID). Finally, spike trains are randomly generated from the resulting rate dynamics. (b) Kinematic model constructed for the same unit. The whisker trajectory and its derivative are fed into a bivariate Gaussian fit of the first-order kinematic tuning map. The output is then used to generate Poisson spike trains. (c) Overall first-order kinematic response of the unit (left) and of its models. (d) Phase response of the unit presented in Fig. 3c and of its models, plotted in polar coordinates. Complex summation of the polar histogram yields the ‘phase vector’ of the response pϕ (arrows, see Methods); the argument of this vector is the preferred phase , and its length is the phase selectivity S. Note that the selectivity of both models is smaller than that of the cell (see Figure 3d). (e) Preferred phases of both models match those of the recorded units (R2=0.88 and 0.94 for LNP and kinematic models, respectively).
(a) Response of exemplary TG cell to synthetic whisking (left), awake playback (middle) and open-loop square wave (right) protocols. Top: cycle kinematics after offset removal and normalization of both amplitude and frequency (bold line is median, shaded area is IQR). Open-loop kinematics, while capturing some basic aspects of whisking, depart from those of natural whisking by having a ‘square wave’ appearance (sharp protraction followed by an epoch of stillness in the fully-protracted state). The kinematic tuning (2nd row), rhythmic tuning (3rd row) and frequency-invariance (bottom row) maps are presented for each protocol. Note the poor coverage of parameter space in the open-loop method. (b) Phase tuning of the cell presented in a, normalized to ease comparison. The phase response is very similar in the two closed-loop protocols but differs for the open-loop case (note the double-peaked curve). (c) The difference in preferred phase between ‘awake-replay’ and synthetic whisking (left) and between open-loop and synthetic whisking (right). The open-loop preferred phase is both more varied (p=0.046, bootstrap, n=22) and biased upward (p=0.006, Wilcoxon signed rank test, n=22). Inset: cumulative distribution functions. (d) Preferred phase of all TG and brainstem units in the awake playback protocol (ordinate) vs. the synthetic whisking protocol (abscissa).
(a) First-order kinematic tuning of an exemplary TG cell. Four restricted loci are marked and numbered. (b) Phase tuning of the cell (blue) and its kinematic model (yellow) in the marked loci. As the model’s firing rate is derived solely from the first-order kinematics (i.e., the location in the map depicted in (a)), it has no phase selectivity within these restricted regions. In contrast, the cell manifests salient selectivity of phases around its preferred phase (~-0.4π). This indicates that other variables, beyond angle and angular velocity, contribute to the cell’s phase selectivity. (c) To quantify the analysis presented in (b), the conditional information content was calculated for each cell and its model using the formula: (i.e., the average phase information conveyed by the cell/model, given the 1st-order kinematic state). The cells had significantly more conditional phase information than their respective models (p<1e-3, Wilcoxon signed rank test for the difference in information, n=41 phase-informative TG cells and their kinematic models). Inset: cumulative distribution of the difference in information.
(a) Parasagittal slice of the rat brainstem showing two recording sites in the ventral PrV, marked by lesions (yellow arrowheads). A penetration track is also visible (blue arrows). (b) Parasagittal slice of the rat brainstem showing three recording sites in the rostral part of SpVi (yellow arrowheads). SpVo: oral subdivision of the spinal trigeminal nucleus; SpVir and SpVic: rostral and caudal parts of the interpolar subdivision. Scale-bar: 1mm.
Supplementary Figure 7 Information processing along the low-level circuits of the rat’s whisking system.
Phase is extracted from the kinematics by follicle mechanoreceptors. Short-term depression (STD) of the synapses leading to both SpVir and PrVm entail high-pass filtering, while the synapses to PrVs retain low-frequency offset information (all-pass filtering). Hence, information on the fast whisker oscillations (rhythmic information) is passed to the paralemniscal pathway via the thalamic posteromedial complex (POm), while both the fast and the slow components of whisking are conveyed to the lemniscal pathway via the thalamic ventral posteromedial nucleus (VPM).
Supplementary Figures 1–7 (PDF 1192 kb)
(PDF 384 kb)
Tracking of whisker protraction angle in an awake, head-fixed rat (left, red) and generation of the same trajectory in an anesthetized rat (right, blue) using real-time closed-loop control. (MOV 1930 kb)
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Wallach, A., Bagdasarian, K. & Ahissar, E. On-going computation of whisking phase by mechanoreceptors. Nat Neurosci 19, 487–493 (2016). https://doi.org/10.1038/nn.4221
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