Responses of cells in the superior colliculus during performance of a spatial attention task in the macaque

Previous studies have reported that superficial layer cells in the superior colliculus (SC) give an enhanced response to a stimulus when it is the target for an eye movement. However, in a peripheral detection paradigm, no such enhancement was found when a stimulus was attended, in the absence of an eye movement. Inasmuch as behavioral studies have found attention deficits in the absence of eye movements following SC lesions or deactivation, we investigated this issue in a paradigm that is very sensitive to effects of attention. In a matching-to-sample paradigm, a sample stimulus was presented at one location followed by a brief test stimulus at that (relevant) location and a distracter at another (irrelevant) location. While maintaining fixation, the monkey indicated whether the sample and the test stimulus matched, ignoring the distracter. The relevant and irrelevant locations were switched from trial to trial. SC cells in the superficial layers tended to give enhanced responses when the attended test stimulus was inside the receptive field compared to when the (physically identical) distracter was inside the field. We found that responses to attended targets in the receptive field were larger than to physically identical, but ignored, distracter stimuli. These effects were found only in an "automatic" attentional cueing paradigm, in which a peripheral stimulus explicitly cued the animal as to the relevant location in the receptive field. No attentional effects were found in a "central" or "cognitive" cueing paradigm, in which the monkey had to learn the relevant location in a given block of trials. The larger responses to attended targets in the automatic cueing paradigm appeared to be due to a sustained elevation of cells' baseline activity when attention was directed to the receptive field, as well as a transient enhancement of the target response. Thus, responses of SC cells appear to be modulated by directed attention, even in absence of eye movements, probably reflecting the properties of cortical cells projecting to the SC.