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Vibrissa motor cortex activity suppresses contralateral whisking behavior

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Abstract

Anatomical, stimulation and lesion data implicate vibrissa motor cortex in whisker motor control. Work on motor cortex has focused on movement generation, but correlations between vibrissa motor cortex activity and whisking are weak. The exact role of vibrissa motor cortex remains unknown. We recorded vibrissa motor cortex neurons during various forms of vibrissal touch, which were invariably associated with whisker protraction and movement. Free whisking, object palpation and social touch all resulted in decreased cortical activity. To understand this activity decrease, we performed juxtacellular recordings, nanostimulation and in vivo whole-cell recordings. Social touch resulted in decreased spiking activity, decreased cell excitability and membrane hyperpolarization. Activation of vibrissa motor cortex by intracortical microstimulation elicited whisker retraction, as if to abort vibrissal touch. Various vibrissa motor cortex inactivation protocols resulted in contralateral protraction and increased whisker movements. These data collectively point to movement suppression as a prime function of vibrissa motor cortex activity.

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Figure 1: Decrease of VMC activity during vibrissal touch.
Figure 2: Decreased activity, decreased excitability and hyperpolarization of VMC during social touch.
Figure 3: VMC activity is additively suppressed by both nose-to-nose touch and whisker protraction.
Figure 4: Unilateral microstimulation of VMC in awake rats leads to contralateral whisker retraction.
Figure 5: Unilateral blockade of VMC increases contralateral whisker movement and protraction.

Change history

  • 17 November 2016

    In the version of this article initially published online, the x axes in Figure 1e,g,i were labeled "Time (Hz)"; the correct label is "Time (s)." Also, the P value in Figure 1j was given as 0.00018; the correct value is 0.0018. The errors have been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank B. Geue, U. Schneeweiß and J. Diederichs for technical assistance and V. Bahr and F. Mielke for assistance with programming. We thank M. Rüsseler for assistance with video tracking and R.P. Rao and E. Bobrov for sharing tracked whisker traces of behaving rats. We thank S. Helgheim Tawfiq for behavior drawings. We thank A. Neukirchner, E. Chorev, S. Ray, P. Bennett and A. Clemens for comments on the manuscript. This work was supported by Humboldt-Universität zu Berlin, the Bernstein Center for Computational Neuroscience Berlin, the German Federal Ministry of Education and Research (BMBF, Förderkennzeichen 01GQ1001A, M.B.) and NeuroCure. M.B. was a recipient of a European Research Council grant and the Gottfried Wilhelm Leibniz Prize.

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C.L.E., G.D. and M.B. designed the study. C.L.E. performed tetrode experiments. C.L.E. and G.D. performed juxtacellular experiments. G.D. and C.L. performed whole-cell recordings. C.L.E. and G.D. performed microstimulation and blockade experiments. C.L.E. analyzed the data and performed statistical modeling. C.L.E. and M.B. wrote the first version of the manuscript. All authors assisted with analyzing data and contributed to writing the manuscript.

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Correspondence to Michael Brecht.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Whisker tracking procedure and additional modeling

(a)Example high-speed (250 frames/s) video frame showing whiskers of a head-fixed rat during a juxtacellular recording experiment. The pivot point (red dot) and the whisker tracking ROI (green dots) are manually clicked for tracking each video.(b)Example traces demonstrating the tracking procedure. We rotated adjacent frames around the pivot point shown in (a) to maximize the correlation between the frames within the whisking ROI (‘Pearson’s ρ‘, top trace) and estimated the mean change in angles between adjacent frames (‘ΔAngle’, middle traces). Datapoints with sudden spikes in the correlation between frames due to video artifacts were removed from the traces (example marked by black arrow). To estimate the whisking angle, we linearly interpolated, numerically integrated and band-pass filtered the change in angle between frames (‘Angle’, bottom trace). Grey bar indicates a nose-to-nose touch.(c)Top: Distribution of βAmpl for all cells is not different from zero (P = 0.204, Wilcoxon signed-rank test, also shown in Fig 3c). Bottom: When we plot only significant cells (assessed by a likelihood ratio test), the pattern is mixed: 10 cells are suppressed (red bars) and 6 cells are activated (blue bars). As a population, they are not different from zero (P = 0.098, Wilcoxon signed-rank test), but we note that the suppressed cells tend to be more strongly modulated that the activated cells: (median |βAmpl|= 0.221/0.128 for suppressed/activated cells, P = 0.00025, Mann-Whitney U-test).(d)Soma of example juxtacellularly labeled Ctip2-negative cell.(e)Example recorded data and fitted model from the neuron shown in (d). The top traces show the occurrence of nose-no-nose touches (grey bars), the juxtacellular recording trace with spikes (high-pass filtered at 300 Hz, top trace) and the whisker angle and whisking amplitude (tracked by high-speed videography). Below we show the estimate of the instantaneous firing rate of the best fitted model (green line, smoothed with a Gaussian with σ = 75 ms) plotted on top of an estimate of the observed firing rate (grey area, calculated by convolving the spike train with a Gaussian with σ = 75 ms, clipped at 10 Hz for plotting). This cell was suppressed by nose touch, whisker protraction and by increased whisking amplitude (maximum likelihood estimates: β0 = 0.03, βNose = −0.70, βAngle = −0.30 (°)-1, βAmpl = −0.38 (°)-1)(f)Fitted betas, when we run the model shown in Fig 3 on stepwise orthogonalized data. In this model, β’Nose measures how the spike rate depends on nose touch, β’Angle measures how the spike rate depends on ‘the variation in whisker angle, which is orthogonal to variations in nose touch’, and β’Ampl measures how the spike rate depends on ‘the variation in whisking amplitude, which is orthogonal to variations in nose touch and variations in whisker angle’. Bars indicate median β, error bars indicate 95% confidence intervals of the median.

Supplementary Figure 2 Unilateral microstimulation of vibrissa motor cortex shortens social facial touch episodes

(a)Cumulative histograms of the duration of social facial interactions (from first to last whisker-to-whisker touch) on days with VMC microstimulation during interactions (red lines) and days with sham stimulation during interactions (black lines) for one example rat.(b)Interactions are shorter with VMC microstimulation than during sham stimulation (N = 4 rats, dots indicate median interaction duration, lines indicate slope (with rat-specific intercept) from LME model, colors indicate rats).

Supplementary Figure 3 Unilateral blockade of vibrissa motor cortex (by AMPA & NMDA antagonists) increases contralateral whisker movement and protraction

(a)Example image of anaesthetized rat after unilateral VMC blockade (right hemisphere) by superfusion of APV (an NMDA antagonist) and NBQX (an AMPA antagonist).(b)Example ipsilateral (blue) and contralateral (red) whisking traces of whisker micromovements, which escape light anaesthesia (Whisker arc 1). The contralateral whiskers are more protracted (~27° vs. ~32°) and the contralateral micromovements have a larger amplitude.(c)After VMC blockade, the whisker set point is higher contralaterally (red markers) than ipsilaterally (blue markers) to the blocked hemisphere (N = 3 rats).(d)After VMC blockade, the whisking power is much higher (~5 fold) in the contralateral whiskers than in the ipsilateral whiskers (Markers indicate ratio of contralateral to ipsilateral whisker power).

Supplementary Figure 4 Unilateral blockade of vibrissa motor cortex (by muscimol injection) increases contralateral whisker movement and protraction.

(a)Top: Example image of lightly anaesthetized mouse after unilateral VMC blockade (left hemisphere) by muscimol injection, showing protraction of contralateral whiskers. Bottom: Example whisking pattern from the same mouse showing large whisker movements contralaterally, and smaller whisker movements ipsilaterally.(b)After VMC blockade, the whisker set point is higher contralaterally (red markers) than ipsilaterally (blue markers) to the blocked hemisphere (N = 4 mice). Round markers indicate that only deep VMC was blocked, square markers indicate that both deep and superficial VMC was blocked.(c)After VMC blockade, the whisking power is much higher (~8 fold) in the contralateral whiskers than in the ipsilateral whiskers (Markers indicate ratio of contralateral to ipsilateral whisker power). Round markers indicate that only deep VMC was blocked, square markers indicate that both deep and superficial VMC was blocked.(d)Example ipsilateral (blue) and contralateral (red) whisking traces of whisker micromovements which escape light anaesthesia (Whisker arc 1) in another mouse, showing the whisking patterns at a longer time scale.

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Ebbesen, C., Doron, G., Lenschow, C. et al. Vibrissa motor cortex activity suppresses contralateral whisking behavior. Nat Neurosci 20, 82–89 (2017). https://doi.org/10.1038/nn.4437

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