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 monkeys, that attention modulates visual signals before they even reach cortex by increasing responses of both parvocellular and magnocellular neurons in the first relay between retina and cortex, the lateral geniculate nucleus (LGN), at the same time it decreases neuronal responses in the adjacent thalamic reticular nucleus (TRN). Francis 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. Thus we find that attention modulates thalamic visual responses in two phases: an initial modulation that enhances LGN responses and attenuates TRN responses, followed by a slowly building later enhancement limited to LGN. Until now, demonstration of attentional modulation of LGN neurons has been limited to preliminary experiments on monkey and fMRI studies in humans. For the TRN, in addition to the recent growth in anatomical and cellular studies of monkey visual TRN, we recently found attentional modulation of neuronal activity in visual TRN during a visual/auditory attention task. The initial LGN modulation might provide a substantial fraction of the modulation seen subsequently in cortical area V1. While it is difficult to compare across studies, the approximately 10% increase in responses we find in LGN is similar to the 7 9% median increase across V1 neurons. The presence of the initial modulation in both TRN and LGN, their reciprocal increase and decrease, and the timing of their visual and attentional responses are consistent with TRN serving as the source of the initial LGN modulation as proposed by Crick. The later attentional effects in LGN, and effects others have reported in higher cortical visual areas, might be more closely related to goal-directed attention which frequently also develops later in the visual response particularly in higher cortical areas. This later modulation in LGN might in fact reflect feedback from cortex onto the LGN via the established connections from V1 layer 6, whereas the initial modulation in LGN by way of TRN may have its origins in subcortical structures. While obviously separate in time course, the two phases of modulation may represent two distinct attentional influences, and may be early indicators for identifying and distinguishing feed-forward and feedback visual attentional mechanisms.
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