A backward progression of attentional effects in the ventral stream

Abstract

The visual processing of behaviorally relevant stimuli is enhanced through top-down attentional feedback. One possibility is that feedback targets early visual areas first and the attentional enhancement builds up at progressively later stages of the visual hierarchy. An alternative possibility is that the feedback targets the higher-order areas first and the attentional effects are communicated "backward" to early visual areas. Here, we compared the magnitude and latency of attentional enhancement of firing rates in V1, V2, and V4 in the same animals performing the same task. We found a reverse order of attentional effects, such that attentional enhancement was larger and earlier in V4 and smaller and later in V1, with intermediate results in V2. These results suggest that attentional mechanisms operate via feedback from higher-order areas to lower-order ones.attention | Macaque | vision | feedback N europhysiologic and brain imaging studies in monkeys and humans have shown that attended stimuli evoke larger responses in visual cortex than unattended distracters (1-6), giving attended stimuli a competitive advantage for representation in the cortex (7). These top-down attentional effects are thought to be mediated in part by feedback from prefrontal and posterior parietal cortex (8-12) acting directly or indirectly on all visual areas in the dorsal and ventral stream, including V1. However, the mechanism of this feedback is unclear. In particular, a first-order question is whether the top-down feedback targets V1 [or even the lateral geniculate nucleus (LGN)] first and then is passed on successively to later areas, or whether it targets higher-order areas first and then is fed back to successively lower areas. Without an understanding of the basic functional anatomy of the attentional feedback, it will be difficult to make progress in unraveling the circuitry for attention.The magnitude and timing of attentional effects on visual responses in all of the different visual structures should, in principle, give insight into the direction of attentional effects along the visual pathways. However, a comparison of the magnitude of attentional effects across visual areas in different studies leads to a confusing picture. On the one hand, imaging studies in humans typically find that attentional effects on evoked responses become larger as one moves from V1 into higher-order areas (13,14). Several neurophysiologic studies in monkeys also often report small (4) or even nonexistent (6, 15, 16) attentional enhancement of firing rates to stimuli in the receptive fields (RFs) of V1 cells (17-19), compared with reliable findings of attentional effects in higher-order areas such as V4 in conventional target detection or discrimination paradigms. On the other hand, other primate studies report substantial attentional effects in V1 in complex tasks such as covertly tracking along curved lines with spatially directed attention (18). It has recently been demonstrated that even with a relatively simple selection task, very large at...

Laminar differences in gamma and alpha coherence in the ventral stream

“…We found a "backward" progression of attentional effects on synchrony in the ventral stream, with the strongest enhancement of synchrony in V4 and the weakest effects in V1, suggesting that V4 might be responsible for the attentional effects in upstream areas through feedback projections (22). Another recent study found an enhancement of gamma synchrony with attention in V4 but a suppression of gamma synchrony in V1 (49).…”

“…Total cells recorded in the superficial layers of V1, V2, and V4 were 67, 13, and 73, respectively, and the corresponding totals in the deep layers were 14, 47, and 12. The superficial V4 cells included 47 cells reported in previous studies of coherence and attention in V4 (1), and individual cells from recordings in all three areas were included in a previous study of attentional effects on firing rate latencies (22). Cells were recorded in two monkeys performing a task of directed spatial attention (Fig.…”

Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey

“…Attentional signals are particularly prominent in V4, influencing 73% of recorded neurons according to the recent study by Buffalo et al (2010). FEF afferents are unusual in forming synapses in all layers of V4.…”

“…The most direct and likely route is the monosynaptic connection from the FEF to the posterior parietal and the occipital lobe (Huerta et al, 1987;Stanton et al, 1995), including area V1 (Clavagnier et al, 2004), V2 (Markov et al, 2011), and V4 (Stanton et al, 1995;Barone et al, 2000). In the occipital lobe, the earliest and strongest effects of the attentional signal are seen in V4, with progressively later and lesser effects in V2 and V1 (Buffalo et al, 2010).…”

Segregated Pathways Carrying Frontally Derived Top-Down Signals to Visual Areas MT and V4 in Macaques

“…In the ventral stream, neurons in visual area 4 (V4) filter irrelevant information from the RF (Moran and Desimone, 1985;Luck et al, 1997). It has also been shown that attentional effects are larger and earlier in V4 than V1 and visual area 2 (V2) (Mehta et al, 2000;Buffalo et al, 2010) and lesions in V4 affect the filtering of distracters at high resolution in downstream area TE (Buffalo et al, 2005). These findings suggest that V4 plays important roles in providing top-down signals to visual areas in the ventral stream.…”