Jack of All Trades: Auditory “Highway” Also Processes Motion

There are some universal truths we learn: the sky is blue, the grass is green, and weekends are never long enough. For neuroscientists, another accepted dogma is that the inferior colliculus (IC) processes auditory signals. Recent research, however, suggests that this might not be the whole story.

A new study from Gunsoo Kim’s group at the Center for Neuroscience Imaging Research in Suwon suggests that the IC, a subcortical area of the brain known to centralize auditory signals, also processes motion information.

The IC can be thought of as a highway for auditory signals. Incoming auditory inputs from the ears and feedback signals from hierarchically higher areas of the brain both converge in the IC.

A striking theme throughout neuroscience research over the past decade is that cortical areas of the brain integrate signals encompassing multiple sensory systems. For example, multiple groups have found that the primary auditory cortex, the earliest site of auditory processing in the cortex, also receives motion information.

So why is it surprising or impactful that the IC may also be modulated by locomotion? The IC is a much more basic, low-level auditory area, whose primary role is to gate information to and from the cortex. Any changes that occur in the IC are sent to higher brain areas, where the motion signals are potentially amplified. Any influence at a low-level brain area, like the IC, is more likely to have effects on behavior.

Think about how often you’re simultaneously moving and listening to something in your environment. Maybe you’re listening to Lizzo while at the gym or to a tour guide while walking around a new city. Humans inherently find themselves in situations involving both motion and auditory sounds. This research could have a major impact on how scientists interpret behaviors in our daily lives.

Changes in all directions

In order to determine if locomotion modulates activity in the IC, researchers recorded extracellular spiking activity from the IC of mice placed on a passive treadmill. Mice could freely choose when to run and when to remain stationary.

The authors first asked, “What does movement do to the IC when we’re not actively listening to anything?” To do so, they measured spontaneous activity in the IC during a period where mice were not exposed to sound stimuli. They compared IC activity when the mice were walking versus stationary and found that 76% of cells had significantly different activity between the two movement conditions (walking and stationary).

Interestingly, the cells with locomotion-modulated activity did not all change in the same way. The vast majority displayed increased activity during the locomotion condition, while the rest showed decreased activity during the locomotion condition.

Anatomy research has shown that the outer portion of the IC receives motor-related projections. Knowing this, the authors examined whether or not the IC cells modulated by motion were grouped at the outer portion of the IC. Anatomical reconstructions showed that the motion-modulated cells were spread throughout the IC, meaning that this effect was not specific to the portion of the IC where locomotion projections terminate.

Locomotion definitely changes activity in the IC, but ironically the changes are all over the map. While you’re walking in silent contemplation, some neurons in your IC become more active while others become less active. The significance of this result on our daily lives is a bit unclear, but one thing is certain – the IC processes both auditory signals and motion. Two modalities humans use almost constantly are integrated from an extremely early point of the auditory pathway through the brain.

Is it really due to locomotion?

But there was one obvious problem – when a mouse runs on a treadmill, the treadmill itself can make sounds. It’s possible that those sounds could be modulating the IC cells, rather than the mouse’s motion. The authors conducted a series of control experiments in hearing-impaired mice to ensure that the differences were due to locomotion, rather than a squeaky mouse treadmill.

They began by verifying that IC cells of hearing-impaired mice are generally less sensitive to auditory stimuli. The slightly deaf mice required a sound of 70+ decibels to show any response, double that of normally-hearing mice. From these experiments, researchers reasoned that any low-level auditory sounds coming from the treadmill would not influence IC activity.

In subsequent testing with the hard-of-hearing mice, the team found that cells in their IC also showed increased or decreased activity during locomotion. This was consistent with their previous results, suggesting that locomotion does indeed modulate activity in the IC.

No one is good at multitasking

Nonetheless, the IC’s primary modality is hearing. The question remained – if the IC is processing sound stimuli, does locomotion still change IC activity? In order to test this, the authors made a small change to their experimental design.

Kim’s group again recorded from the IC while mice ran or remained still on a treadmill. However, for this set of experiments, researchers also presented various tones during each motion condition.

The authors identified IC cells that responded to presented auditory tones. Upon further investigation, they found that 72% of those cells had a significantly different response to the auditory tone while the animal was in motion. Importantly, they found that almost all of the locomotion-modulated cells had a smaller response to the presented tone during the locomotion condition compared to when the animals were stationary. In fact, this change was so dramatic, that IC cells’ responses to tones during locomotion were only two-thirds the size of their response when the mice remained still. Despite the fact that locomotion can cause increases or decreases to spontaneous activity, when IC cells are processing auditory tones, their responses are decidedly attenuated during locomotion.

If it seems like listening to your friend is more difficult as your stroll through a park, rather than sitting at a café – here’s your excuse!

It’s all relative – paradoxically improved hearing

Previous research has shown that decreased response gain, like the decrease seen in the locomotion condition, suggests that cells are less able to signal their preferred frequency. Specific IC cells generally prefer certain tones. So while IC cell A may prefer tones at 8 kHz, and cell B may prefer tones at 16 kHz, neither increase their activity to represent the 4 kHz frequency. The authors examined if the functional ability of cells to signal their preferred frequency changed between motion conditions.

Kim’s group found that the preferred frequency for each cell remains the same regardless of whether or not the mouse is moving. Importantly, they found that the dynamic range that cells use to relay frequencies changes between the two locomotion conditions. Although moving decreases activity at all frequencies, the decrease disproportionately affects the frequencies that cells care less about.

This disproportionate reduction in non-preferred frequencies increases the dynamic range between frequencies that the cell prefers and disregards, actually increasing cells’ ability to reliably signal their preferred frequency. Future studies are needed to determine if the computational improvement in sensitivity is robust enough to affect perception.

You’re back in the park, and your friend is talking while you walk and watch some ducks. The decreased activity in your IC makes it harder to detect if a duck is quacking or not. But the fact that the decreased activity disproportionately affects irrelevant frequencies makes it easier for you to discriminate the words your friend is telling you. Sadly, it seems this research isn’t an excuse for not paying attention after all.