The process of visual attention has been likened to a searchlight that illuminates a particular region within one’s visual field, leaving the rest relatively dim. Precisely how the brain achieves this fundamental feat has long been a mystery. Now, however, researchers at the National Eye Institute have described experiments in monkeys that show one of the more important ways in which the searchlight process works. Their data, published online Oct. 5 in Nature, appear to confirm a well-known hypothesis by the late Nobel-winner Francis Crick, who proposed that attention modulates sensory information even before it gets to the cortex.
“It’s another case of Francis having made a proposal that 10 or 20 years later is found to be true; he has a remarkable track record,” says Christof Koch, a neuroscientist at the California Institute of Technology who has worked in this area, with Crick among others.
Without the enhancing and filtering effects of attentional processes we could never cope with all the data flooding in through our senses. The sets of processes known as “executive attention” or “cognitive control,” for example, appear to originate in the frontal cortex, where higher-order goals and concepts are stored. Through vast networks of nerve fibers, these processes extend their influence to other, “lower” areas of the cortex where relatively raw sensory inputs are handled.
Crick, the co-discoverer of DNA who turned to neuroscience in later life, proposed in a paper in 1984 that attention’s reach extends even outside the cortex, to a way station between the sensory organs and the cortex known as the thalamus. “While on the face of it the thalamus appears to be a mere relay, this seems highly unlikely,” Crick wrote. “Its size and its strategic position make it very probable that it has some more important function.”
Crick hypothesized that attention-related signals operate on sensory data via a part of the thalamus known as the reticular complex: “If the thalamus is the gateway to the cortex, the reticular complex might be described as the guardian of the gateway.”
That hypothesis was left essentially unproven for the next 24 years. Recent experiments with people, using functional magnetic resonance imaging (fMRI), have provided some evidence that thalamic neurons, including the lateral geniculate nucleus (LGN), where the optic nerve terminates, are modulated by attention. But, says Koch, “from previous animal experiments the assumption has been that attention doesn’t really affect LGN that much, and affects primary visual cortex not so strongly.”
How attention affects the optic nerve
In the Nature study, neuroscientists Kerry McAlonan and her husband, James Cavanaugh, working with lab director Robert Wurtz at the National Eye Institute, have shown in experiments in monkeys that Crick’s hypothesis appears to be true at least for visual attention.
“We have confirmed that neuronal responses in the LGN increase with attention,” says McAlonan. “It’s much like the attentional modulation observed in the cortex by other researchers.”
McAlonan and her colleagues trained three macaque monkeys to perform a visual attention task and then wired parts of their thalamuses with electrodes. They found that whenever the monkeys attended to an image in a segment of their visual field, the activity of LGN neurons responsive to that part of the visual field went up – too quickly to have been influenced by the visual cortex.
How did the attentional signal get to the LGN? Following Crick’s lead, McAlonan and her colleagues looked at a nearby structure called the thalamic reticular nucleus (TRN). This structure is wired to the LGN in such a manner that each TRN neuron communicates in both directions with a corresponding LGN neuron.
When TRN neurons are active, they inhibit the activity of their corresponding LGN neurons. McAlonan and her colleagues found that when the monkeys became attentive to a stimulus, the TRN was affected too, becoming less active for stimulus-related neurons and thus—by reducing its inhibition of the LGN—allowing the corresponding LGN neurons to become more active. This attentional effect was measurable in the TRN about four milliseconds before it appeared in the LGN, suggesting that—as Crick predicted—the TRN delivers the attentional signal to the LGN, and thus serves as “the guardian of the gateway.”
McAlonan and her colleagues are now trying to trace this TRN-mediated attentional circuit to its origin. They suspect that it operates via a midbrain structure known as the superior colliculus, which is involved in the planning and generation of eye movements.
“Given that shifts of attention are often followed by eye movements to the attended location, it’s not unreasonable to believe that these two functions are linked,” she says.