Neural enhancement and pre-emptive perception: the genesis of attention and the attentional maintenance of the cortical salience map

One of the stable hypotheses in systems neuroscience is the relationship between attention and the enhancement of visual responses when an animal attends to the stimulus in its receptive field (Goldberg and Wurtz, 1972 Journal of Neurophysiology 35 560-574). This was first discovered in the superior colliculus of the monkey: neurons in the superficial layers of the superior colliculus responded more intensely to the onset of a stimulus during blocks of trials in which the monkey had to make a saccade to it than they did during blocks of trials in which the monkey had to continue fixating a central point and not respond to the stimulus. This enhancement has been found in many brain regions, including prefrontal cortex (Boch and Goldberg, 1987 Investigative Ophthalmology 28 Supplement, 124), V4 (Moran and Desimone, 1985 Science 229 782-784), and lateral intraparietal area (Colby et al, 1996 Journal of Neurophysiology 76 2841-2852; Colby and Goldberg, 1999 Annual Review of Neuroscience 22 319-349), and even V1 (Lamme et al, 2000 Vision Research 40 1507-1521). In these studies the assumption has been that the monkey attended to the stimulus because the stimulus evoked an enhanced response. In the experiments described here we show that for abruptly appearing stimuli, attention is not related to the initial response evoked by the stimulus, but by the activity present on the salience map in the parietal cortex when the stimulus appears. Attention to the stimulus may subsequently, by a top down signal, sustain the map, but stimuli can as easily be suppressed by top down features as they can be enhanced.