Cortical crosstalk

By Jef Akst Cortical Crosstalk Scientists are eavesdropping on the brain’s conversations in search of clues underlying complex behaviors. Recorded waveforms of neural activity. Courtesy of Earl Miller The brain is the most complex organ in the human body, but for years, available technology greatly limited scientists’ interpretation of how the billions of neurons act in concert to create complex behav

Oct 1, 2009
Jef Akst

Cortical Crosstalk

Scientists are eavesdropping on the brain’s conversations in search of clues underlying complex behaviors.

Recorded waveforms of neural activity.
Courtesy of Earl Miller

The brain is the most complex organ in the human body, but for years, available technology greatly limited scientists’ interpretation of how the billions of neurons act in concert to create complex behaviors. Recent advances in neuronal recording technology, however, along with the invention of the Pentium processor–based computer capable of digitizing the data at a much higher rate than ever before, have enabled brain research to progress at an increasingly rapid pace.

In 2007, neuroscientist Earl Miller of the Massachusetts Institute of Technology and his postdoc Timothy Buschman pushed the evolving technology to a new level with rhesus macaques. By implanting up to 50 electrodes, which recorded activity from neurons in three different brain regions simultaneously, the study (this month’s Hot Paper) was one of the first to compare entire populations of neurons from multiple areas of the primate brain. As the monkeys performed different visual search tasks, the researchers compared the activity of neurons in the parietal and frontal cortices. They found that in search trials where the item the monkeys were looking for was extremely obvious—so-called bottom-up processing—the parietal cortex reacted first, followed by the frontal cortex. In contrast, when the monkey must actively search for the target—so-called top-down processing—the signal flowed in the opposite direction.

A few years earlier, neuroscientists Michael Goldberg and James Bisley of Columbia University in New York had found that the parietal cortex was involved in both top-down and bottom-up processing,1 “but we didn’t know which way [the signal] was going,” says Bisley, who currently works at the David Geffen School of Medicine at the University of California Los Angeles. The 2007 study was the first to demonstrate such directionality in attention-related behavior.

While Miller wasn’t the first to record from multiple areas in the primate brain simultaneously, he “really pushed the envelope” with regard to the number of electrodes, says neuroscientist Bob Desimone of the Massachusetts Institute of Technology. “[Using] multiple electrodes [to] record from different [primate] brain regions made this study a major step forward,” agrees neuroscientist John Duncan of the MRC Cognition and Brain Sciences Unit (CBU) in England.

Since the publication of this month’s Hot Paper, the use of multielectrode recording has spread like wildfire through the primate neuroscience community. “It certainly started something that I think has been very good for the field,” Bisley says. “I wouldn’t call [the technique] common, but I think everyone is trying to get going in that direction.”

Scientists are now using multielectrode approaches to tackle a wide range of complex topics, including attention, coordination, and decision making. “There are hardly any primate labs that aren’t playing around with multielectrode recording in some way,” says Desimone.

Rats to macaques

The use of multiple electrodes in different regions of the mammalian brain began in the mid-1990s, when researchers employed the technique to shed light on the precise relationships between groups of neurons.

In 1995, neuroscientist Miguel Nicolelis of Duke University Medical Center permanently implanted dozens of hair-like electrodes—known as microwires—to concurrently record from five different brain areas of rats. He identified predictable cycles of synchronized activity during tactile stimulation and just before the rats’ whiskers started exploring their environment.2

In 1998, Nicolelis used his microwires to record from three different cortical regions of owl monkeys, all of which showed nearly simultaneous activation upon tactile stimulation.3 Starting in 2001, Desimone and his colleagues published a series of studies in which they used multiple, movable electrodes to record neuronal activity within the visual areas of macaques.4 All of this laid the foundation for Buschman and Miller’s 2007 paper, and a concurrent study by neuroscientist Trichur Vidyasagar of the University of Melbourne.5

The new wave

Other neuroscientists have since used Buschman and Miller’s technique to further explore how different brain regions work together to coordinate behavior. In 2008, neuroscientist Bijan Pesaran of New York University and colleagues recorded the frontal and parietal cortices in rhesus macaques and learned that the two areas were more in sync when monkeys had freedom to make their own choices versus when they had to follow instructions, suggesting these areas may be part of a “decision circuit.”6 In May of this year, Desimone’s group found that the frontal eye fields—an area believed to respond to visual stimuli—and the V4 area of the visual cortex showed a similar pattern of activity when a monkey was presented with colored dots on a screen. This finding suggests that communication between these two areas may play a role in attention.7 Most recently, Buschman and Miller published a study demonstrating that coordinated activity within the frontal eye fields may help regulate when monkeys shift their attention while performing difficult search tasks.8 Scientists have also begun to use multielectrode techniques to understand the intricate neural signals necessary for controlling prosthetic limbs.

“It’s pretty clear that a lot of labs are very excited about the potential that [multiple electrodes] have,” Pesaran says. Multielectrode recording is “the tool of the future,” Nicolelis agrees. “In a few more years, we’ll be able to record [30,000] or 40,000 cells [simultaneously].”

Data derived from the Science Watch/Hot Papers database and the Web of Science (Thomson ISI) show that Hot Papers are cited 50 to 100 times more often than the average paper of the same type and age.

T.J. Buschman and E.K. Miller, “Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices,” Science, 315:1860–62, 2007. (Cited in 90 papers)
1. J.W. Bisley et al., “Neuronal activity in the lateral intraparietal area and spatial attention,” Science, 299:81–86, 2003.
2. M.A.L. Nicolelis et al., “Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system,” Science, 268:1353–58, 1995.
3. M.A.L. Nicolelis et al., “Simultaneous encoding of tactile information by three primate cortical areas,” Nature Neuroscience, 1(7):621–30, 1998.
4. P. Fries et al., “Modulation of oscillatory neuronal synchronization by selective visual attention,” Science, 291:1560–63, 2001.
5. Y.B. Saalmann, “Neural mechanisms of visual attention: how top-down feedback highlights relevant locations,” Science, 316:1612–15.
6. B. Pesaran et al., “Free choice activates a decision circuit between frontal and parietal cortex,” Nature Letters, 453:406–9, 2008.
7. G.G. Gregoriou et al., “High-frequency, long-range coupling between prefrontal and visual cortex during attention,” Science, 324:1207–10, 2009.
8. T.J. Buschman et al., “Serial, covert shifts of attention during visual search are reflected by frontal eye fields and correlated with population oscillations,” Neuron, 63:386-96, 2009.