In the previous post, I briefly discussed the background and methods behind this paper by Ritt et al.. In this post I summarize and discuss the main results. I just noticed that Neuron added the apt banner, "What the rat's vibrissa tell the rat's brain" to the article.
Ex vivo whiskers
As I discussed in the previous post, the resonance hypothesis is the claim that the resonance frequencies of whiskers provide an ethologically important channel of information about what is going on in the world of the rat. Subsequent papers, however, have argued against the resonance hypothesis, as they were unable to reproduce whisker resonance in a more ethologically realistic preparation in which a whisker is fixed at a base and moved across a fixed surface (this is a little odd, since Hartmann already showed that resonance occurs in whiskers of awake behaving rats).
The first set of experiments in the paper addressed these issues, monitoring whisker movement as a whisker was brushed against a fixed surface at different speeds. They did observe resonance, as expected, but found an interesting twist--resonance wasn't prominent at every speed, but at a relatively narrow range of speeds, a 'hot spot' (see Figure 1B of the paper, shown below, which shows whisker angular velocity traces when the whisker is moved across the same surface at different speeds). This hot spot is thought to be within the range of speeds that whiskers move in ethological contexts, so it could be that rats exploit resonance during certain tasks by moving their whiskers at the appropriate speed.
In situ whiskers
The majority of the paper examined the micromotions of whiskers while rats performed a texture discrimination task. The task was relatively simple: the rat runs into a chamber that contains two different textures along the wall--a rough texture and a smooth texture (think of it as rough and smooth sandpaper). The rats are trained to get reward by running to a door that corresponds to a particular texture (e.g., when the smooth texture is on the right, enjoy a reward when you move to the right).
Their high-resolution monitoring of the whisker motions revealed a very interesting pattern to the movements. A whisker will slip along the surface, and then stick to a particularly abrasive feature, staying in place as the rat continues to move its head. Then, after the tension grows enough, the whisker whips forward (slips) before sticking at another spot further along (for example, see the clip from Figure 3 below: the top panel shows the trace of a whisker during the trial, and the bottom panel shows the angle (red) and position (blue) of the whisker). This is often accompanied by a kind of 'ringing' of the whisker as it sticks in place. Perhaps not surprisingly, this slip-n-stick pattern occurrs more often when it sweeps along the rough surface.
In the frequency domain, the mean frequency of movement of each whisker was inversely proportional to whisker length. This suggests that the elasticity that confers different resonance frequencies upon whiskers of different lengths also influences the frequency of whisker vibrations during the present discrimination task (the figure below, clipped from the paper, shows an example of the likelihood of different frequency components in two whiskers of different length).
While the frequencies of oscillation were consistent with resonance frequencies observed ex vivo, the rats didn't seem to sample the textures with all of their whiskers, which they might do if their goal was to maximize the information about frequency available from whiskers of different lengths (e.g., the "whiskers as cochlea" picture may need to be tweaked). Indeed, the largest two arcs of whiskers rarely touched the textured surface.
Among other things, their analysis also revealed a unique signature of rough-surface contact: a set of high velocity, large amplitude whisker deflections that were not seen in previous studies. Figure 8 of the paper provides a scatter plot that includes the rise time (roughly, time from trough to peak of a whisker movement) and velocity of whisker movements, and those events that were both high velocity and longer in duration (signifying higher amplitude) were much more likely to occur during contact with the rough surface.
Where are we?
This paper, a heroic effort that has established a great method and some intriguing results, is only the beginning. The whisker coding literature is finally catching up to vision when it comes to understanding the inputs to this system. Many more experiments are needed, not just to examine the role of resonance in transmitting information about the world, but to determine the role of different types of whisking patterns the rat employs as it scurries about.
Apropos of the resonance hypothesis, it would be interesting to see how rats fare when their whiskers are cut so they are all the same length. This should decrease the differences in resonance frequencies in different whiskers. Hence, to the extent that resonance is important for a task, we would expect to see their performance compromised (note, though, things are a little more complicated: resonance frequency depends on other factors than length). It will also be crucial to measure which micro-features of whisker movement are tracked neurally in awake behaving rodents.
This paper has opened up possibilities beyond just the resonance hypothesis. It reveals the slippery, sticky, messiness that is present when rats use their wonderful keratinous appendages to explore their world.
Acknowledgments:: Thanks to Jason Ritt for clarifying an important point about the velocity 'hot spot' mentioned in the ex vivo experiments.