Distinct modes of visuo-spatial attention in macaque V1 and V4.

Sharma, J.^1,2, Sugihara, H. ¹, Schummers, J. ¹ and Sur, M. <sup>1, 2

1</sup> Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge MA, USA
² Martinos Center for Biomedical Imaging, Mass. General Hospital, Charlestown MA, USA

Psychophysical studies suggest that spatially directed attention mediated by both top-down and bottom-up processes can improve perceptual sensitivity to an attended location. While the top-down control is goal-directed and deployed voluntarily, the bottom-up component is stimulus driven. The stimulus driven component should therefore engage neurons in primary visual cortex (V1) at the onset of attentional process whereas the voluntary, top-down component should initially engage V4 and higher areas. However, most physiological studies find robust modulation with attention in V4 neurons and only a weak, delayed modulation of V1 neurons, that is taken as the signature of top-down mediation of attention. In an ongoing series of experiments, we have examined spatial and temporal dynamics of attentional modulation in V1 and V4 by using a reverse-correlation technique. This approach, employed in simultaneous recordings of V1 and V4 neurons, has helped us study attentional dynamics on a millisecond timescale. Two monkeys were trained to covertly attend to a small attention spot that could appear near the receptive field (RF) of a neuron or away from it in the contralateral hemifield.  The spot could extinguish after a random interval following which the monkey had to release a bar within 350-400 ms to earn a juice reward. The stimuli, consisting of patches of sinusoidal gratings at 8 different orientations, two different contrasts and two sizes, were flashed at 75 Hz. Identical stimuli were presented overlapping the RF and in the contralateral location, while we recorded from neurons in V1 and V4.  We find that attention towards the receptive field shows distinct modes of response modulation in V1 and V4. Whereas V4 neurons show strong modulation early on when the animal allocates covert attention towards the RF, no such modulation was seen in V1. However, V1 neurons show clear modulation when attention is required to achieve a behavioral goal that culminates in a motor response. Neurons in V4 also show similar modulation, but this modulation follows V1 responses in time. Furthermore, attention delays contextual influences in V4 but does not influence their magnitude. In V1, attention accentuates contextual influences: a suppressive surround becomes more suppressive whereas surround facilitation gets more facilitated with attention.