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It's Neuron Time

Investigators seek the tick and tock of the brain's clock | By Jack Lucentini

 

British novelist Aldous Huxley in a bid to study perception supposedly taped his conversations after swallowing the hallucinogenic drug mescaline. During one such chat, a researcher asked him to describe how time felt. "There seems to be plenty of it," was all Huxley could offer.1

Silly as that sounds, few have done much better in explaining time or its sensation. Yet scientists are taking the first stabs at answering at least one part of the question: how the brain perceives time. For example, a University of Washington study is the first to document how neurons in primates track time from one instant to the next.2 And even in a research field where no one knows what to expect, the investigations are turning up surprises.

The findings cast some doubt on an idea that appeals to many, that the brain has an internal "clock" that somehow ticks ceaselessly away, providing a single reference frame for thoughts and actions.3 Instead, some researchers contend, time may be represented in many brain areas in a manner suited to each area's particular functions and inseparable from the decisions made there. Other researchers say the brain may use the same circuitry, or cells, to measure time, space, and magnitude.

MONKEY SHINES Time perception's physical basis has been little studied, perhaps "because the abstract dimensions of our experience--time, space, and number--are so far removed from the elementary sensations,"4 wrote Charles R. Gallistel, a professor of psychology at Rutgers University in Piscataway, NJ. But this is changing, says Deborah L. Harrington, research scientist at the Veterans Affairs Medical Center in Albuquerque, N. Mex. "Timing is a subject of increasing interest, because it's important in learning," she says. Learning skilled movements, for instance, involves internalizing their sequences and timing.

The University of Washington team found that certain monkey neurons showed a gradual, ramp-like rise or fall in activity correlated with the animal's judgment of elapsed time. Monkeys were trained to observe how long a light flashed and then asked to decide whether a second flash was longer or shorter. Most flashes were several tenths of a second long. The monkeys signaled their answers by looking at one of two colored dots on a screen. Meanwhile, researchers recorded signaling in individual neurons using intraneuronal microelectrodes. They identified two opposite patterns of neuronal response. One was a gradual increase or ramping up of activity during the test flash. If a neuron becomes active as the animal prepares to look at the colored dot, that space in which the dot appears is said to be in the neuron's response field. A neuron's response pattern depended on whether or not the dot was in its response field.

The ramping pattern would happen quickly or slowly depending on the length of the first flash. The neurons also tended to follow Weber's Law, an established concept that people's timing errors are proportional to the duration being timed. More severe errors were made when the flashes were longer. The neurons were probably gauging time, they concluded.

Yet, individual neurons were rather imprecise at timing, with only about 70% accuracy, according to investigator Matthew I. Leon. Monkeys themselves achieved much better accuracies of 90%, probably because the brain makes decisions based on neuronal populations, averaging out individual inaccuracies.

"Individual cells behave like noisy timers," says Leon, now a postgraduate researcher at the University of California, Irvine. "You'd have a hard time performing a task well by listening to one neuron." The brain is known to measure other things the same way. In gauging a moving object's direction, for example, the brain combines many neuronal responses for an accurate judgment. While this aspect was consistent with previous findings, others were less self-evident.

THE PATH TO INTENTIONS The researchers hinted at a strong link between timing and decision-making. The neurons didn't just track time, Leon says; they indicated the changing likelihood that a particular eye movement would occur, as modulated by time. "The neurons are telling us about elapsed time semi-independently of the ensuing eye movement."

Reprinted with permission from Elsevier Science

 TIMED RESPONSES: After a neuron's response field was determined, a monkey was presented with a time-discrimination task. A central, blue fixation point turned white for either 316 or 800 ms (standard cue). After a delay, the cue again turned white for a variable period (the test cue). Following a second delay, the fixation point disappeared and the monkey looked at one of the two peripheral targets. (Neuron, 38:317-27, 2003)

The investigators found neurons that make this link because they chose cells from a brain area they already knew to be responsible for planning eye movements: the posterior parietal cortex. This suggests that other brain regions, such as cortical areas that mediate reaching motions, contain similar timing neurons. "We don't think we just got lucky and that the 'internal clock' just happens" to be in the area studied, Leon says.

The findings also indicate that "timing is wrapped up within intentions," says Michael N. Shadlen, University of Washington and Leon's coauthor. "We do things according to a time scale: 'By now I should do this, by now I should have my hand here.'" The timing neurons identified may have a broad range of intention-related activities, adds Shadlen. Neurons in the area appear to represent abstract qualities such as "an evolving conviction, belief, or the weight of evidence favoring a particular proposition, so long as that proposition is going to be communicated by an eye movement to a target in that neuron's response field."

Shadlen speculates that timing neurons located throughout the brain would make a central clock unlikely. "Suppose you had a neuron that's a perfect clock, say, ticking off action potentials every few milliseconds. Then other neurons elsewhere in the brain would have to mark those clock ticks. Then you wouldn't need the clock at all."

CENTRAL TIME Vincent Walsh, of the Institute of Cognitive Neuroscience at University College London, proposes that time, space, and magnitude are encoded in identical neural circuitry.5 The brain area Leon and Shadlen studied contains neurons reported to respond to all three properties, he wrote.1 Indeed, says Walsh, a single neuron may encode all three, though not necessarily simultaneously. Psychology research supports the concept, he adds. Two studies have found that people judge time to pass more quickly when they work with small-scale model environments, such as train sets.6,7 And, Walsh adds, children mix up time and space frequently: "It's only when you teach children special stories like The Tortoise and The Hare that they start to learn that faster doesn't mean farther."

Walsh concedes he doesn't know how the multifunctional brain cells would work, but some answers might be found in a recent imaging study in monkeys by Hirotaka Onoe and colleagues at the Osaka Bioscience Institute in Japan.8 They found that time monitoring depends on a network comprising the posterior inferior parietal cortex and the dorsolateral prefrontal cortex. Both areas may contain multifunctional neurons, Walsh wrote,5 but with different functions. Unlike the former region (the one Leon and Shadlen also studied), the dorsolateral prefrontal cortex "seems to be important in a lot of memory functions" as well as in planning-sequencing actions like brewing a cup of tea, Walsh says.

The basal ganglia9 and cerebellum10 also are implicated in timing tasks. The basal ganglia seem to "detect time information stored in all areas of the executive cortex, then use it to regulate the execution of movements," says Harrington. The cerebellum may serve as something akin to a central clock for time scales under a second, contends Eliot Hazeltine, assistant professor of psychology at the University of Iowa. For instance, he says, "If you know you want to close your eyes half a second after hearing a tone, a signal from the tone is sent to the cerebellum."

Leon says he doesn't see strong evidence for a centralized, dedicated internal clock, but it might turn up. If not, he adds, something similar might, such as neurons that only encode time, unencumbered by the spatial associations of the cells he identified. To ferret out such pure time neurons, he says, a researcher might conduct a study similar to his own, except the monkey wouldn't be instructed where to look until after the duration to be judged has passed. That way "you've isolated the time demands of the task from the spatial demands," he explains. There may be no need to resort to mescaline after all.

Jack Lucentini (jekluc@aol.com) is a freelance writer in New York City.

References
1. V. Walsh, "Time: the back-door of perception," Trends Cogn Sci, 7:335-8, August 2003.

2. M.I. Leon, M.N. Shadlen, "Representation of time by neurons in the posterior parietal cortex of the macaque," Neuron, 38:317-27, 2003.

3. M.A. Conditt, F.A. Mussa-Ivaldi, "Central representation of time during motor learning," Proc Natl Acad Sci, 96:11625-30, 1999.

4. C.R. Gallistel, "Time has come," Neuron, 38:149-50, 2003.

5. V. Walsh, "A theory of magnitude: common cortical metrics of time, space, and quantity," Trends Cogn Sci, in press.

6. A.J. DeLong, "Phenomenological space-time: toward an experiential relativity," Science, 213:681-3, 1981.

7. C.T. Mitchell, R. Davis, "The perception of time in scale model environments," Perception, 16:5-16, 1987.

8. H. Onoe et al., "Cortical networks recruited for time perception: a monkey positron emission tomography (PET) study," Neuroimage, 13:37-45, 2001.

9. I. Nenadic et al., "Processing of temporal information and the basal ganglia: new evidence from fMRI," Exp Brain Res, 148:238-46, 2003.

10. P. Thier et al., "Encoding of movement time by populations of cerebellar Purkinje cells," Nature, 405:72-6, 2000.