Unraveling circuits of visual perception and cognition through the superior colliculus

The spatial interaction of visual attention and saccadic eye movements was investigated in a dual-task paradigm that required a target-directed saccade in combination with a letter discrimination task. Subjects had to saccade to locations within horizontal letter strings left and right of a central fixation cross. The performance in discriminating between the symbols "E" and "E", presented tachistoscopically before the saccade within the surrounding distractors was taken as a measure of visual attention. The data show that visual discrimination is best when discrimination stimulus and saccade target refer to the same object; discrimination at neighboring items is close to chance level. Also, it is not possible, in spite of prior knowledge of discrimination target position, to direct attention to the discrimination target while saccading to a spatially close saccade target. The data strongly argue for an obligatory and selective coupling of saccade programming and visual attention to one common target object. The results favor a model in which a single attentional mechanism selects objects for perceptual processing and recognition, and also provides the information necessary for motor action.

The posterior parietal cortex (PPC) plays an important role in many cognitive behaviors; however, the neural circuit dynamics underlying PPC function are not well understood. Here we optically imaged the spatial and temporal activity patterns of neuronal populations in mice performing a PPC-dependent task that combined a perceptual decision and memory-guided navigation in a virtual environment. Individual neurons had transient activation staggered relative to one another in time, forming a sequence of neuronal activation spanning the entire length of a task trial. Distinct sequences of neurons were triggered on trials with opposite behavioral choices and defined divergent, choice-specific trajectories through a state space of neuronal population activity. Cells participating in the different sequences and at distinct time points in the task were anatomically intermixed over microcircuit length scales (< 100 micrometers). During working memory decision tasks the PPC may therefore perform computations through sequence-based circuit dynamics, rather than long-lived stable states, implemented using anatomically intermingled microcircuits.

Accurate saccadic programming in natural visual scenes requires a signal designating which of the many potential targets is to be the goal of the saccade. Is this signal controlled by the allocation of perceptual attention, or do saccades have their own independent selective filter? We found evidence for the involvement of perceptual attention, namely: (1) summoning perceptual attention to a target also facilitated saccades; (2) perceptual identification was better at the saccadic goal than elsewhere; and (3) attempts to dissociate the locus of attention from the saccadic goal were unsuccessful, i.e. it was not possible to prepare to look quickly and accurately at one target while at the same time making highly accurate perceptual judgements about targets elsewhere. We also studied the trade-off between saccadic and perceptual performance by means of a novel application of the "attentional operating characteristic" (AOC) to oculomotor performance. This analysis revealed that some attention could be diverted from the saccadic goal with virtually no cost to either saccadic latency or accuracy, showing that there is a ceiling on the attentional demands of saccades. The links we discovered between saccades and attention can be explained by a model in which perceptual attention determines the endpoint of the saccade, while a separate trigger signal initiates the saccade in response to transient changes in the attentional locus. The model will be discussed in the context of current neurophysiological work on saccadic control.