Guarding the gateway to cortex with attention in visual thalamus

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Abstract
The striking effects of shifts of attention are well illustrated by the behaviour of children with attention-deficit hyperactivity disorder. It is thought that attentional effects arise in the thalamus, but for the visual system it has proved difficult to determine precisely where the earliest stages of sensory processing take place. McAlonan et al. now demonstrate in experiments on macaque monkeys that spatial attentional modulation takes place in the lateral geniculate nucleus, and opposing effects in the adjacent thalamic reticular nucleus that makes inhibitory connections onto it. This reciprocal activity may be a mechanism for generating transient attention, in confirmation of a proposal made by Francis Crick nearly 25 years ago when his interests shifted from DNA to neuroscience. He hypothesized that a spotlight of attention was directed by a tiny nucleus in the brain, the thalamic reticular nucleus. It was thought that attentional effects arise in the thalamus but for the visual system, evidence at the single cell level has been rare. This paper demonstrates spatial attentional modulation in primate lateral geniculate nucleus as well as opposing effects in the adjacent thalamic reticular nucleus, which makes inhibitory connections onto it. The massive visual input from the eye to the brain requires selective processing of some visual information at the expense of other information, a process referred to as visual attention. Increases in the responses of visual neurons with attention have been extensively studied along the visual processing streams in monkey cerebral cortex, from primary visual areas to parietal and frontal cortex1,2,3,4. Here we show, by recording neurons in attending macaque monkeys (Macaca mulatta), that attention modulates visual signals before they even reach cortex by increasing responses of both magnocellular and parvocellular neurons in the first relay between retina and cortex, the lateral geniculate nucleus (LGN). At the same time, attention decreases neuronal responses in the adjacent thalamic reticular nucleus (TRN). Crick5 argued for such modulation of the LGN by observing that it is inhibited by the TRN, and suggested that “if the thalamus is the gateway to the cortex, the reticular complex might be described as the guardian of the gateway”, a reciprocal relationship we now show to be more than just hypothesis. The reciprocal modulation in LGN and TRN appears only during the initial visual response, but the modulation of LGN reappears later in the response, suggesting separate early and late sources of attentional modulation in LGN.

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