The Universal Sense (12 page)

As usual, the limitation for understanding the behavior of a species with calls outside our own range was based on two factors. First is the problem of treating bats as sonar machines rather than complex animals living in a complex world. This is a normal if unfortunate outgrowth of translational research—it’s hard to keep all the actions of something as dynamic as a mammal in mind when you’re trying to represent them through equations and hard data. The second problem is that to understand animals that hear outside of our range, we need to use technological and experimental tools that change over time, hopefully giving better results as they get more complex, rather than just cluttering up the datascape. While the discovery that bats could determine changes in echoes shorter than a microsecond happened in the early 1990s, and arguments about it raged until just a few years ago, when better digital technology confirmed the findings multiple times, the underlying basis for bats’ temporal hyperacuity only began coming to light in the last few years and required better molecular techniques than were available back in the day. Bats’ ability to determine the timing of echo structure turns out not to require superpowers—just a developmental feature probably caused by an evolutionary mutation that was retained longer in bats than other small mammals, and only identifiable now, after great strides in brain research.

When the brain of a mammalian fetus is developing, it forms connections based on patterns of gene expression. Our DNA turns on and off numerous chemical signals that cause the cells to differentiate into specific cell types following what’s called
their
fate map
and migrate from the place of their birth to specific sites in the developing brain. But when the newly born and positioned neurons start connecting up, they lack the neurochemical complexity that makes the postnatal brain responsive to changing environmental conditions. Many developing neurons connect not with modifiable chemical synapses but rather with
gap junctions
, small channels that directly connect one neuron to another, allowing precise and rapid flow of signals between the neurons. This is useful for laying down early patterns of connectivity in the brain. But most of these gap junctions are replaced by chemical synapses as the brain develops, with only a few regions in the brain retaining them into adulthood. And none were ever seen in the central auditory system of a mammalian brain until 2008, when because of a shipping error, I received a small vial of antibody to connexin-36 (Cx36), the protein that makes up neuronal gap junctions, instead of the neural tracer I actually ordered. Antibodies are widely used in studying brain chemistry because they will latch onto a specific protein, and if you process them with a fluorescent marker, you can generate extremely colorful and precise maps of how that protein is distributed in the brain.

Rather than ship it back (it would have spoiled), I decided to try to see how Cx36 was distributed in a bat’s brain compared to a mouse’s brain. It turned out that for the most part, a bat’s Cx36 distribution looked very much like a mouse’s—the few regions that normally express the gap junction protein in adult mice were all lit up. But something looked wrong. The region where the auditory nerve first enters the brain, called the anteroventral cochlear nucleus (AVCN), was so brightly labeled that it was the brightest part of the brain, but only around the area that first contacted the entering auditory nerve fibers.
When I looked closer, it turned out that the label was in a very specific group of cells that seemed to form an interconnected network. This network was positioned right where they could affect the first auditory signals coming into the brain. Further experiments showed that they were cells not only full of connexins in their surface but also labeled with gamma amino butyric acid or GABA, the neurotransmitter that causes inhibition of other neurons. The clincher was that these cells, when labeled with a neuronal tracer, didn’t actually project to the rest of the auditory system—they seemed to be set up to only act on either auditory nerve fibers or the first processing neurons that did send projections up through the brain.

We had found the biological equivalent of a temporal filter—something that lets only precisely timed signals enter the brain—and it’s never been seen in other animals. The way we think it works is that the cochlea sends bundles of nerve fibers from regions that respond to similar frequencies. Since the mammalian ear is made of wetware rather than silicon and wires, there is a certain degree of slop in the time of arrival of signals from the cochlea, even from nerve fibers that may be only microns apart or infinitesimally shorter or longer than their neighbors. And while at the time of writing this book this is still under investigation, what appears to happen is that bats, by some evolutionary mutation that let them retain this fetal feature, develop a network-based filter at the lowest part of the auditory system that only allows the first signal from any given frequency to get through. This spectrotemporal gateway means that their auditory system isn’t any faster than a mouse’s or a human’s—it’s just much more precise. They don’t have to be super-organisms or violate the law of physics to create images from sound; they are
merely the product of their particular evolutionarily driven development.

But what can we learn from bats that is translational—that directly relates to human hearing? While bats have been the inspiration for technological advances from sonar to ultrasound, their ultra-precise hearing seems a form of evolutionary exotica that has little to do with how humans hear. But it turns out that bats may hold the secret to a problem that plagues all of us as we age: presbycusis, or age-related hearing loss. We humans, like all mammals, lose our hearing as we age, even if we didn’t spend years in front of high-powered speakers or under headphones or working in loud environments. It’s always been treated as a normal part of the aging process, but it underlies a lot of serious cognitive and behavioral problems, such as the loss of ability to understand speech in even normal acoustic environments, and may be the basis for some of the paranoia associated with Alzheimer’s and other dementias. It’s easy to think that something is going on behind your back when you can no longer monitor the world out of your line of sight. The basic theory has been that since the hair cells at the base of the cochlea (the narrowest part, near the oval window) are closest to the outside world, they take the greatest beating from acoustic input, whether “normal” sounds such as speech or potentially damaging noise such as blasts or chronic exposure to subway noise. Since mammals, unlike frogs, don’t regenerate auditory hair cells under normal circumstances, the high-frequency-sensing hair cells will be the first to wear out.

But there is a serious problem with this theory. It’s all well and good to suppose that forty years of sound will start wearing out the structure, but mice, who live only a year or two and are
one of the most common models for auditory function, start showing high-frequency hearing loss after about a year, with certain mutants showing symptoms in only a few months. So the issue is clearly more complicated than what a manufacturer would call normal wear and tear; there have been hundreds of studies examining various genes and gene products that seem to be involved (although not clearly causative) in high-frequency hearing loss. So we are looking at a complicated system that seems to be a universal problem in mammals. Or is it? The answer may lie in the bat’s ear and brain.

Echolocating bats live an uncommonly long time. My favorite big brown bat, Melanie, was about sixteen when she died. There are documented cases of little brown bats (
Myotis lucifugus
) living to thirty-four years. This is ridiculously long for a small mammal with a high metabolism. A bat eats its weight in insects every day, and a hunting bat’s heartbeat can reach 1,000 beats per minute—a rate that would make a human heart explode. If you follow normal metabolic models, bats should live three to four years. Even if you give them time off for hibernation, they still live three times longer than they should.
²⁰
And yet these animals are absolutely dependent on high-frequency hearing. A deaf bat not only will slam into things but will starve to death because it can’t hunt. Somehow, bats have evolved an auditory system that preserves at least the most critical range of their hearing necessary for echolocation, which for big brown bats starts at about 20 kHz and for little brown bats starts at about 40 kHz, and keeps it functional for years longer than any other known mammal could. And we have no idea why.

Whenever I hear some student bewailing the fact that with the thousands of papers on hearing (and everything else in science) appearing annually, it seems like we’ve discovered everything, I just smile and shake my head and begin asking him or her all the questions we don’t know the answer to. Do bats lose the extreme upper end of their hearing and just retain the low end, implying that this is merely a scaling function for their auditory range? Or do they have some molecular or systemic method for keeping their hair cells healthy? Or do they, like fish, frogs, and birds, have the ability to regenerate hair cells that are damaged? The list of things we don’t know goes on for a very long time. Echolocating bats, which seem so exotic and strange, even to other auditory scientists and animal behaviorists, may hold the secret that will allow humans to have healthy hearing for their entire lives. We just have to figure out the right questions.

Chapter 5
What Lies Below: Time, Attention, and Emotion

A few years ago when I lived in southern Rhode Island, I went for a nighttime run. When I run during the day, I usually put on some headphones and run to something with a decent beat, partially to mask traffic noise and partially to give me an external basis for my pace.
²¹
But when I run at night, I leave the music off and just listen to the environment. The lack of sunlight makes the sounds much richer, and you’re also safer being able to hear everything going on around you. I was on a downhill part near some favorite ponds, usually rich with the sounds of bullfrogs and green frogs trying to get lucky. But shortly after I turned onto the road and ran past the first of them, I noticed that they were quieter than usual, even after I had thunderfooted past. I kept running and started hearing what sounded like very soft footsteps, so I stopped, jogging in place, and looked around.

The road, aside from a single streetlight near a quarry a few hundred yards away, was dark, real
country
dark. Dark in a way that, as a recently transplanted New Yorker, I was just learning to cope with. But there was nothing there, and I didn’t hear anything else, so I moved on toward the next pond. The frogs shut up on schedule as I got around a hundred feet away, but I thought I heard the padding sound again. At this point I was beginning to get a little nervous, so I did another stop and search; all was quiet. I decided that since I wasn’t somewhere sensible like Brooklyn, where there are streetlights for illumination and bodegas to step into in the event of trouble, I would pick up the pace. Just as I was about to bolt toward the streetlight, I heard a loud splash and a snarl. I jumped several hundred feet straight up (okay, it might have been a few inches) and swiveled around to face the pond, my whole body tense and ready to run whichever way the source of the noise wasn’t. What I saw was the sorriest, most bedraggled and shamefaced coyote imaginable. He must have been pacing me for the last quarter mile or so and, like his cartoon counterpart Wile E. Coyote, run right off the edge of the sidewalk and dropped straight into the pond, leaving him soaked in both water and the coyote equivalent of embarrassment. He jumped out of the pond, shook himself dryish, and slunk off, muttering under his breath. I couldn’t help myself—I said “meep meep” and ran off in the other direction.

This story shows why it’s important not to wear headphones when you’re in the dark: because hearing communicates more to you than just what’s in your iTunes playlist, or even the sounds in your immediate vicinity. It lets you monitor the world around you even out of your line of sight and in the dark, and it does it faster than any of your other senses. Your brain is a pattern-seeking machine, constantly identifying relationships between
all the sensations and perceptions that bombard you. Sensory inputs that are correlated in some way—by similar frequency, timing, timbre, or location (or, in the non-auditory world, shape, color, flavor, or smell)—cause neurons to fire in similar patterns at or nearly the same time. Neurons that fire in synchrony are more likely to trigger their target neurons to fire, hence passing the message “Something non-random happened” further up to the executive processing regions of your brain. Since your perceptions are based on binding common elements of sensory input together in time and space, other senses such as vision that are spatially limited and relatively slow often get false positives when correlating heavily overlapping or ambiguous features. This is why there are so many web pages devoted to cool optical illusions, and so few that even mention auditory illusions—it’s harder to trick your ears. Hearing tends to be better at segregating inputs properly even though it gathers information from a much wider region, unlimited by line of sight. This is because hearing is faster than vision.

At first, thinking of hearing as faster than vision seems counterintuitive. We are used to assuming that our brain and vision are really fast—witness phrases such as “fast as thought” (about 750/1,000 second, according to one Johns Hopkins study) or “gone in the wink of an eye” (about 300/1,000 second). Sounds fast, and compared to the amount of time it’s taken you to read this paragraph, it is. But it’s all relative. Consider a few examples: the quartz crystal in an old-style watch oscillates at 32,000 times per second; our atomic clocks are set to the vibration rate of a single energized cesium-133 atom, more than 9 billion oscillations per second; iodine atoms vibrate 1 million billion times a second; and quarks exist for only a yoctosecond (10−
²⁴
second), meaning you would have to go to 2 × 10−
²¹
quark births and funerals in the time it took to notice that there was something stuck under your contact lens. Luckily, we are tuned to operate on a much more limited time reference scale, from a few tenths of a second to our own life span, which is, sad to say, only about 2.5 × 10
⁹
seconds even if you do go to the gym regularly.