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Enhancement by spatial attention would ideally be expected to be dominant at the pre-saccadic target representation until just before the saccade begins, and decay at or soon after the saccade ends. Similarly, attentional enhancement would be expected to emerge at the post-saccadic target representation at or soon after the saccade ends.
In other words, if attentional enhancement of the pre-saccadic target representation decayed well before the saccade, or attentional enhancement of the post-saccadic target representation emerged well after the saccade, there would be time-periods where the target stimulus did not receive the benefits of attentional allocation.
Contrariwise, if attentional enhancement of the pre-saccadic target representation lingered after the saccade, or attentional enhancement of the post-saccadic target representation emerged pre-emptively well before the saccade, attention would be peri-saccadically allocated to irrelevant spatial locations, distractor processing would potentially be facilitated and this would degrade task performance.
Until now, to our knowledge, the time-course of the shift of attentional modulation from the pre-saccadic to the post-saccadic target representation across a saccade has not been explicitly measured. In the only previous physiological recording study on this issue, using a saccade task similar to ours with a fixed attentional target, object-based attentional enhancement of multi-unit activity in monkey V1 was reported to emerge in the post-saccadic target representation approximately 80 ms after the end of the saccade 4.
However, this study did not measure the dynamics of the decay of attentional enhancement in the pre-saccadic target representation. On the other hand, in a human imaging study, functional magnetic resonance imaging fMRI and electroencephalogram EEG data from humans have been taken as evidence for attentional modulation lingering for about ms after the saccade in the pre-saccadic target representation; 5 an interpretation supported by results from human psychophysical studies 6 , 7.
Human psychophysical data consistent with an early, pre-saccadic emergence of attentional modulation in the post-saccadic target representation have also been reported 8 , 9.
This psychophysical inference of pre-emptive attentional modulation in the post-saccadic target representation is consistent with a large body of single-neuron recording data from putative attentional control regions in monkeys showing that neurons in the lateral intraparietal area, superior colliculus and frontal eye field 3 , 10 , 11 , 12 respond predictively when a stimulus was expected in their receptive field RF after the saccade.
This predictive activity is greater in the lateral intraparietal area LIP for stimuli with greater bottom-up saliency 13 and for stimuli that are learnt visual search targets 14 or saccade targets Though these results are suggestive see Discussion , they do not address the time-course over which attentional enhancement is remapped from the pre-saccadic to the post-saccadic target representation across a saccade.
In order to measure the time-course of this trans-saccadic attention shift, we trained two monkeys to make saccades while maintaining attention on a moving random dot pattern RDP at a fixed spatial location. We recorded from visual area MT, a key locus in the cortical motion-processing pathway of humans and monkeys, where neurons show both small RFs and clear, robust, attentional enhancement 15 , 16 , 17 , We show for the first time that the trans-saccadic shift of attentional enhancement is well synchronized to saccades and that attentional enhancement crosses over from the pre-saccadic to the post-saccadic target stimulus representation soon after saccade offset.
We recently showed that in humans performing a similar task, spatial attention is fully available at the task-relevant location within 30 ms after the saccade Taking visual response latency into account see Discussion , this rapid post-saccadic availability of spatial attention at the task-relevant location in humans is in excellent agreement with the physiological time-course of trans-saccadic attention shifts in monkeys that we report here.
Our results show that the trans-saccadic attention shift in primates is precisely co-ordinated with the saccade to maintain attentional enhancement on relevant stimuli, so that they can be attentionally enhanced soon after the beginning of each eye fixation and can thus be optimally tracked and processed across saccades. Results Peri-saccadic attentional task Our experimental paradigm required monkeys to maintain attention on one of four moving RDPs while also making a saccade; we refer to this attended RDP as the target and the other three as distractors.
We recorded from neurons in area MT during this task. In Experiment 1, we estimated the attentional enhancement of the pre-saccadic target representation, while in Experiment 2, we estimated the attentional enhancement of the post-saccadic target representation.
To do this, in Experiment 1, we placed the attended RDP so that before the saccade, it lay either in the RF the attend-in condition or meridionally opposite to it the attend-out condition : we measured the attentional enhancement of the pre-saccadic target representation by comparing the firing-rates in the attend-in and attend-out conditions upper part of Fig.
In contrast, in Experiment 2, we placed the attended RDP so that after the saccade, it lay either in the RF the attend-in condition or meridionally opposite to it the attend-out condition : we now measured the attentional enhancement of the post-saccadic target representation by comparing the firing-rates in the attend-in and attend-out conditions lower part of Fig.
Stimulus X is foveated before the saccade and stimulus Z after the saccade. The attended stimulus Y falls in the RF of neurons representing retinal location a before the saccade and in the RF of neurons representing retinal location b after the saccade.
An initial spatial cue marked the target location on each trial. The target change occurred between and ms after RDP onset. Before the saccade, neurons respond more strongly to a target stimulus cyan curve compared to a distractor stimulus magenta curve. PSTHs constructed by filtering the spike-trains with a truncated Gaussian window 15 ms standard deviation, ms filter width stepping every 1 ms see Methods.
Inset rectangles: cue location for the two conditions. Left to right: first dashed vertical line—mean time of RDP onset, second dashed vertical line—mean time of fixation point jump, dotted vertical line—mean time of saccade onset.
The early response before RDP onset in the attend-in condition cyan curve is the cue response. Data are pooled from both monkeys. After the saccade, neurons respond more strongly to a target stimulus blue curve compared to a distractor stimulus red curve Full size image Peri-saccadic attentional response dynamics Based on prior findings 17 , 20 , we expected to see an attentional enhancement of the pre-saccadic target representation in Experiment 1 before the saccade and of the post-saccadic target representation in Experiment 2 after the saccade.
This is indeed what we found. We defined and estimated the attentional enhancement as the difference in firing-rates between attend-in and attend-out conditions. For the pre-saccadic target representation in Experiment 1, there is significant attentional enhancement in the time-window from 0— ms before saccade onset Monkey H: 5.
For the post-saccadic target representation in Experiment 2, there is significant attentional enhancement in the time-window from 0— ms after saccade offset Monkey H: 6. These results confirm, as expected, that an attentional response enhancement is found in the pre-saccadic target representation before the saccade, and in the post-saccadic target representation after the saccade.
Our primary goal was to characterize the time-course of this shift of attentional enhancement from the pre-saccadic to the post-saccadic target representation and measure how well this shift was synchronized to the saccade. To do this, we focused on the time-interval from ms before to ms after saccade offset during which the attention shift takes place Fig.
For best task performance, the attention shift should happen as close to saccade offset as possible so that the pre-saccadic target representation is enhanced right up until saccade offset and the post-saccadic target representation soon after saccade offset. The attentional enhancement of the post-saccadic target representation Experiment 2 becomes statistically significant right after saccade offset in monkey H and after 50 ms of saccade offset in monkey E black curves in Fig.
Comparing the two representations directly, the attentional effect in the post-saccadic target representation becomes larger than the attentional effect in the pre-saccadic target representation at 29 ms monkey H and 53 ms monkey E after saccade offset; we call this time the attentional cross-over time. To estimate the variability of this cross-over time, we used a bootstrap procedure to calculate an inter-quartile range IQR: see Methods : the IQRs were 10 ms monkey H and 11 ms monkey E.
The cross-over times calculated using a ms standard-deviation Gaussian-filtered PSTH are very close to those obtained using a smaller standard deviation of 10 ms monkey H: 28 ms and monkey E: 54 ms. The proximity of the attentional cross-over to saccade offset indicates that the attention shift is well synchronized to the saccade, after taking the visual response latency of MT neurons into consideration see Discussion.
Importantly, we did not find any evidence for predictive attention shifts in MT: there is no attentional enhancement of the post-saccadic target representation before saccade offset black diamonds in Fig.
This is particularly notable because unlike earlier studies 18 , 21 , we made sure that there was a stimulus in the RF before the saccade. The presence of this stimulus ensured a stimulus-driven response on which a putative predictive attentional signal could act, and rules out the argument that the apparent absence of a predictive response is simply because the predictive attentional signal does not modulate spontaneous activity in MT.
Finally, in a series of additional control analyses, our conclusions about the rapid post-saccadic dynamics of attention shift remain robust when matching for firing-rate across neurons in Experiments 1 and 2 Supplementary Fig. Data are for monkey H in a and for monkey E in b. Gray and black curves show the mean difference and s. Diamonds above the curves indicate the successive, non-overlapping 50 ms time-bins in which the differences are significantly larger than zero one-sided t-test : black diamonds for the black curve and gray diamonds for the gray curve.
The gray curves in a and b are computed as the difference between the cyan and magenta curves in c and d, respectively, while the black curves in a and b are computed as the difference between the blue and red curves in e and f, respectively. Yao will certainly make you closer to exactly what you want. Yao will be always good friend at any time.
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