Inner Workings: Inside the mind of a jumping spider

At first, there were explosions. Neurobiologists investigating the peculiar behavior of the jumping spider sought to record its neurons. But the scientists’ method always spelled doom for the creatures: peeling back the spiders’ exoskeleton to expose the brain caused vital fluids to burst forth.

New brain recording techniques should help reveal the neurobiological underpinnings of the jumping spider’s complex behaviors. Image courtesy of Tsevi Beatus, Gil Menda, and Paul Shamble (Cornell University, Ithaca, NY).

For decades, neurobiologists and ecologists have struggled to understand just how the poppy seed-sized brains of jumping spiders gave rise to one of the richest behavioral repertoires among arachnids. But a research team recently discovered a minimally invasive way, using superstrong electrodes, to reach the spider brain without major surgery (1). The technical breakthrough has opened a new frontier of neurophysiology, allowing scientists to record brain activity while spiders detect, track, and decide how to respond to their prey and potential mates.

Members of the jumping spider family (called Salticidae) stand out among spiders for their sharp vision. Four pairs of eyes form a turret around the animal’s head that provides a near-360° world view. The two largest eyes, placed front and center, detect color and fine details, and the remaining eyes serve as low-resolution motion detectors that help orient the animal to objects of interest.

Unlike web-spinning spiders that wait for food to land in their webs, jumping spiders use their specialized visual system to actively stalk and pounce on their prey. The hairy arachnids often scuttle along circuitous routes to avoid detection, tackling their target from above. Female jumping spiders also size up the gyrations and gesticulations of males performing courtship dances.

“There are a lot of hypotheses about how jumping spiders are able to do these complex things,” says Damian Elias, who studies jumping spiders at the University of California, Berkeley. Finally being able to record from the spiders’ neurons will be a game-changer, he says. “It’s actually going to let us test those hypotheses about their cognitive abilities.”

A Delicate Touch

Spiders had long been thought inaccessible to neural recordings because their bodies are filled with pressurized fluids. As they are pumped from one chamber into another, the fluids help spiders move their limbs to walk, run, or jump. But that internal hydraulics system poses a technical challenge for neurobiologists.

Glass electrodes, typically used to record from invertebrate neurons, are too fragile to poke through the spider’s exoskeleton. Researchers had tried to surgically expose the brain first, opening windows through which to insert the electrodes. The spiders didn’t fare well.

“Once you poke a hole in it, the blood squirts out and the animal dies within a few seconds or a minute,” says Cornell University neurobiologist Ronald Hoy, whose team pioneered the new technique. “That was a challenge.”

Hoy’s group used a much stronger tungsten electrode typically used in vertebrates, such as mice and monkeys. Inserted carefully, these probes could push directly through the spider’s body into the brain without the need for extra cuts.

To prepare the spiders for neural recording, the researchers first put the naturally skittish animals in the refrigerator for a few minutes to slow them down. Then, with a pair of forceps, they loaded the spiders—which range from a few millimeters to just over 10 millimeters in length—into a custom 3D-printed plastic harness positioned in front of a video screen. Strategically placed dabs of wax secured the animals in place (Movie S1).

When the researchers pushed the tiny tungsten filament through the spider’s exoskeleton, the wound was small enough (about 150 micrometers around) that only a tiny bead of fluid escaped, which sealed into a clot around the electrode and stabilized the preparation. “That prep was the real breakthrough,” says Elias, a former graduate student of Hoy’s.

Starting to See

Initially, Hoy’s team had little available neuroanatomical data to tell them where to guide their electrodes. They used external landmarks, such as subtle changes in coloration and the placement of particular hairs on the spider’s body, to aim roughly for a brain region called the arcuate body, hypothesized to be a visual processing center. “The first few times we did it, we weren’t necessarily in the right place, but we were just happy to be in the brain,” says Hoy.

The group recorded many neurons at first that did not respond to visual stimuli. But the researchers moved their electrodes from one site to another. And, by trial and error, they homed in with greater precision on a patch of neurons that burst with activity when the spiders viewed video images of flies—their natural prey—moving back and forth. The same neurons responded less to pictures of other spiders and to digital mash-ups of fly parts. It’s too early to know whether the neurons are dedicated solely to recognizing flies, says Hoy, but at least these initial results suggest that individual spider neurons can pick out ecologically relevant signals.

Scientists still don’t have a clear picture of how the spider’s tiny brain circuits incorporate signals from each of the eight eyes to produce such a rich repertoire of behavior. But if future studies can provide insights, Hoy sees potential applications: for example, helping engineers design miniaturized robots with multiple cameras or sensors.

And there could be implications for basic neuroscience. Just as scientists’ early neural recordings in the squid in the mid-1900s helped uncover the nature of the action potential—the basic unit of electrical signaling in all neurons—recordings in spiders could help scientists understand how groups of neurons work together.

“Now we’re at the point of trying to understand how neurons are interconnected and how the interconnectedness of them is able to lead to complex behaviors,” says Elias. “Jumping spiders are going to be a great model for studying complex behaviors.”