Getting intimate with rat whiskers (2): Ritt et al.

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.

Getting intimate with rat whiskers (1): Ritt et al.

This is the first of a two-part post on the recent Neuron paper Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats by Jason Ritt and others in Christopher Moore's group. They provide a much-needed high-resolution look at the the movement of whiskers in freely-moving rats as they perform a discrimination task.

Where's the neuroscience?
Before describing the main results, I'd like to discuss why, as neuroscientists, we should care about what whiskers are doing. "Where is the neuroscience?" someone may ask of a paper that just examines whisker movements. To that I would respond, "What is the stimulus?" The first rule of psychophysics and sensory coding is, "Know thy stimulus" (it was EJ Chichilnisky that hammered this into my mind). Students of psychophysics and sensory coding try to quantify the relationship between the stimulus and some other variable (either behavior (psychophysics) or neuronal activity (sensory coding)), so we need to precisely quantify the stimulus on each trial to make sure we have all the relevant information contained in the stimulus.

Because of such concerns, the question we should be asking is why researchers studying coding in the whisker system know so little about what the whiskers are doing, given the importance of understanding the stimulus in sensory coding and psychophysics. In the present paper, Ritt et al. provide a much-needed corrective to this deficit.

The resonance hypothesis
For a few years now, Moore (and Mitra Hartmann at Northwestern) have been pointing out that whiskers are not simple passive detectors of what goes on in the world. Rather, whiskers have interesting intrinsic properties that shape their responses as the rat scurries about palpating the world.

For example, each whisker has a resonance frequency. If you attach a stimulator to the end of a whisker and move it at frequencies, there is a 'hot spot' at which the whisker will vibrate with a significantly higher amplitude. The following figure (Figure 2 from Niemark et al) shows the amplitude of a whisker's movement as a function of stimulation frequency. The breakaway images show data from individual frequencies (gray line: stimulus, black line: whisker movement downstream from the stimulus):


This whisker in the figure has a resonance frequency just under 400 Hz. The resonance frequency of a whisker depends on that whisker's length (longer whiskers have lower resonance frequencies). Interestingly, the length of whiskers increases quite significantly as you move from the front to the back of a rat's face.

As an interesting historical aside, the possiblity that whiskers have resonance frequencies was initially noticed by Niemark while she was still an undergraduate working with John Hopfield. Then the idea was fleshed out experimentally by Niemark, Moore and Mark Andermann (leading to this paper) and by Mitra Hartmann and others at Cal Tech (leading to this paper). The present paper is the latest in a series of papers from Christopher Moore's group exploring the consequences of whisker resonance.

Getting back to the science, what is the significance of all this resonance business? Is it possible that whiskers with different resonant frequencies are induced to resonate by different types of stimuli? This is part of what has become known as the resonance hypothesis (review here). As described in the original paper by Niemark and others, "vibrissa resonance is optimally positioned to increase the range of detection and the specificity of discrimination, and may provide the ability to represent complex stimuli through a compact, somatotopically distributed code" (p 6500).

Many of us think of the resonance hypothesis as the 'whiskers as cochlea hairs' hypothesis. It has been a quite productive idea for experimentalists, and it is interesting to note that it wasn't even on our radar until Neimark asked a simple question: what are the properties of the sensor used by the rat?

Resonant oscillations have been observed in detached whiskers (image above) and in the whiskers of anesthetized rats. It has also been shown that cortical neurons respond differently when a whisker is stimulated at its resonance frequency (see the above review of the resonance hypothesis). But is whisker resonance ethologically important?

Does resonance really matter? Why it is hard to answer this question
A key question is whether resonance is important in the awake freely moving rat performing a discrimination task. One step toward anwering this question is to determine whether resonance is observed in the whiskers in a particular task. If not, then resonance cannot be used so we'd have evidence that resonance is irrelevant for that task.

So, what's the problem? Measure the whiskers in awake freely moving rats and get on with it. Unfortunately, it turns out to be extremely difficult to track tiny whisker movements in a rat that is running around moving its body, head, and whiskers any old place it wants. You need to get the optics just right to see many of these wispy whiskers in focus, use a high-speed camera (the resonance frequencies can be higher than 500 Hz), and then set up a system to automate the tracking of the whiskers (no way you are going to code all that data by hand with the required large fields of view and fast frame rates). It would be a herculean effort.

Mitra Hartmann, presently at Northwestern, chipped away at this problem a bit. She analyzed some interesting video data from the awake freely moving rat in this paper where whisker movements were sampled between 250 and 1000 Hz. She observed that whiskers often exhibit resonant oscillations after contacting an object, but not when the rat is simply whisking in open air.

But what about when a rat is performing a stimulus discrimination task? Could resonant oscillations actually be used to discriminate the features of an object such as its texture? To get at such questions, Ritt et al have pushed things much further. They have developed algorithms to automatically track the entire length of individual whiskers during a texture discrimination task in freely moving rats. They capture images at the impressive frame rate of 3000 Hz. Here's one example from Figure 3 of their paper:
Here they show the results when a single whisker is tracked (it shows the shape of the whisker over multiple frames into the past in red) as the rat moves its head across a surface that changes from rough to smooth texture (you can think of it as moving from rough to smooth sandpaper). To someone interested in sensory coding and psychophysics in the whisker system, this image is simply a symphony.

So what did they observe? To give away the punchline, it seems resonance is present during the task. But there is enough cool stuff in the paper that I'll put off the discussion of the results and interesting open questions to Part 2.

Acknowledgements Many thanks to Mitra Hartmann and Christopher Moore for explaining some of the history of the resonance hypothesis and for clarification of some key points.