Dynamics of attention shifts in frontal eye fields and primary visual cortex as revealed by simultaneous recordings

Models of attention are based on the notion that top-down signals from frontal cortex influence the processing of information in early visual areas (Desimone and Duncan, 1995). The manner, through which such a putative interaction occurs, however, is not clear. We recorded the neuronal activity in the frontal eye fields (area FEF) and the primary visual cortex (area V1) while monkeys were performing a curve tracing task, which requires shifts of attention. In order to monitor neuronal interactions under different attentional demands we manipulated the task difficulty. We characterized the effects of attention by measuring the strength and the latency of attentional modulation in these areas. An increase in task difficulty resulted in reduction of strength and increased latencies of the attentional modulation in each area. We found that attentional modulation in area FEF was stronger than in area V1. The latency of modulation was, however, not significantly different between these two areas, which suggests they jointly participate in the attentional selection process during curve tracing. We also measured the correlation between the strengths of responses of neurons within area V1 and between V1 and area FEF. This so-called rate-covariation was stronger between pairs of recording sites within area V1 than across the two areas. The interareal rate-covariation between area FEF and V1 was stronger if the same curve fell in neurons' receptive fields compared to when different curves fell on the receptive fields. Moreover, the rate-covariation between neurons in different areas that coded the same curve was significantly affected by attention and task difficulty, being strongest when an easy stimulus that was attended stimulated the receptive fields. The pattern of rate-covariation points to an intricate communication network between FEF and V1 that is flexibly modulated by behavioural context.