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 cortex1–4. 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 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.

The major pathway for visual information reaching cerebral cortex is through the lateral geniculate nucleus (LGN) of the thalamus. Acting on this vital relay is another thalamic nucleus, the thalamic reticular nucleus (TRN). This nucleus receives topographically organized collaterals from both thalamus and cortex and sends similarly organized projections back to thalamus. The inputs to the TRN are excitatory, but the output back to the thalamic relay is inhibitory, providing an ideal organization for modulating visual activity during early processing. This functional architecture led Crick in 1984 to hypothesize that TRN serves to direct a searchlight of attention to different regions of the topographic map; however, despite the substantial influence of this hypothesis, the activity of TRN neurons has never been determined during an attention task. We have determined the nature of the response of visual TRN neurons in awake monkeys, and the modulation of that response as the monkeys shifted attention between visual and auditory stimuli. Visual TRN neurons had a strong (194 spikes/s) and fast (25 ms latency) transient increase of activity to spots of light falling in their receptive fields, as well as high background firing rate (45 spikes/s). When attention shifted to the spots of light, the amplitude of the transient visual response typically increased, whereas other neuronal response characteristics remained unchanged. Thus, as predicted previously, TRN activity is modified by shifts of visual attention, and these attentional changes could influence visual processing in LGN via the inhibitory connections back to the thalamus.

SUMMARY A critical technique for understanding how neuronal activity contributes to behavior is determining whether perturbing it changes behavior. The advent of optogenetic techniques allows the immediately reversible alteration of neuronal activity in contrast to chemical approaches lasting minutes to hours. Modification of behavior using optogenetics has had substantial success in rodents, but has not been as successful in monkeys. Here we show how optogenetic inactivation of superior colliculus neurons in awake monkeys leads to clear and repeatable behavioral deficits in the metrics of saccadic eye movements. We used our observations to evaluate principles governing the use of optogenetic techniques in the study of the neuronal bases of behavior in monkeys, particularly how experimental design must address relevant parameters, such as the application of light to subcortical structures, the spread of viral injections, and the extent of neuronal inactivation with light.

Active vision requires integrating information coming from the retina with that generated internally within the brain, especially by saccadic eye movements. Just as visual information reaches cortex via the lateral geniculate nucleus of the thalamus, this internal information reaches the cerebral cortex through other higher order nuclei of the thalamus. This review summarizes recent work on four of these thalamic nuclei. The first two pathways convey internal information about upcoming saccades (a corollary discharge) and probably contribute to the neuronal mechanisms that underlie stable visual perception. The second two pathways may contribute to the neuronal mechanisms underlying visual spatial attention in cortex and in the thalamus itself.