Guarding the gateway to cortex with attention in visual thalamus

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 cortex. 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). Crick 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. We recorded responses of LGN and TRN neurons in three awake behaving macaque monkeys. Monkeys were directed by a central cue at the point of fixation to attend to one of two peripheral visual stimuli on randomly interleaved trials (Fig. 1a inset). One of these stimuli was in the receptive field (RF) of the recorded neuron. Figure 1a shows the responses of an example magnocellular LGN neuron (LGNm) to a light bar within the RF when attention was directed out of the RF (dashed curve, ATTout) or into the RF (solid curve, ATTin). Responses shown are from correct trials. The ATTin response falls above the ATTout response, indicating an increase in neuronal response with attention. The mean response to the same stimulus increased 12% with attention. Figure 1b shows the responses of a parvocellular LGN neuron (LGNp) that also increased (21%) when attention was directed into the RF. If a similar increase in attention were to occur in TRN, however, Crick’s hypothesized interaction between TRN and LGN encounters a problem: TRN inhibits LGN. The visual sector of TRN receives excitatory inputs from LGN, but projects modulatory inhibitory input back to LGN. Therefore, TRN responses should instead decrease with attention, reducing the inhibitory influence of the TRN on LGN, thereby causing the increase in the responses of LGN neurons that we observe. We did in fact find a decrease in the TRN visual response with attention (Fig. 1c). When attention was directed into the RF of this TRN neuron, the mean response to the same visual stimulus was 13% less than when attention was directed out of the RF. We have summarized the effect of attention on mean visual responses of 57 on-centre LGN neurons (19 LGNm and 38 LGNp) in Fig. 2a, and of 29 TRN neurons in Fig. 2b. In each plot, the ordinate is the baseline ATTout response and the abscissa is the attentional modulation, ATTmod. ATTmod can be expressed either as the contrast measure (ATTin2ATTout)/(ATTin1ATTout), or the ratio of modulation (ATTin/ATTout). We have included both, with the