Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4

Abstract

Attention typically amplifies neuronal responses evoked by task-relevant stimuli while attenuating responses to task-irrelevant distracters. In this context, visual distracters constitute an external source of noise that is diminished to improve attended signal quality. Activity that is internal to the cortex itself, stimulus-independent ongoing correlated fluctuations in firing, might also act as task-irrelevant noise. To examine this, we recorded from area V4 of macaques performing an attention-demanding task. The firing of neurons to identically repeated stimuli was highly variable. Much of this variability originates from ongoing low-frequency (<5 Hz) fluctuations in rate correlated across the neuronal population. When attention is directed to a stimulus inside a neuron's receptive field, these correlated fluctuations in rate are reduced. This attention-dependent reduction of ongoing cortical activity improves the signal-to-noise ratio of pooled neural signals substantially more than attention-dependent increases in firing rate.

Figure 1. Attention task

Each trial began with fixation of a central point. While fixation was maintained, one or two of four identical Gabor stimuli were cued with a brief luminance increase. All four stimuli then moved along independent randomized trajectories that brought one stimulus into the receptive field. All stimuli then paused for 1000 ms. Stimulus locations were then shuffled a second time and motion terminated. The fixation point then disappeared. Reward was delivered if a saccade was made to each target and no distracters.

Figure 2. Example Neuron showing an attention-dependent reduction in response variability

Raster plots, in which tic marks indicate the times of spikes, are shown from 48 trials in which the stimulus placed inside the receptive field trials was attended (trials highlighted in red box) and 48 more trials, in which the stimulus was ignored (trials highlighted in blue box). The leftmost yellow vertical line indicates the time in each trial when the stimulus paused in the receptive field while the second yellow line marks the time at which it began to exit the receptive field. At the bottom, the Fano factor (variance spike counts across trials divided by the mean) is shown computed in 100 ms counting intervals spaced over the duration of the trial. The variability was significantly reduced when the stimulus was attended (red) compared to ignored (blue). Error bars +/− 1 SEM.

Figure 3. Single unit examples showing attention-dependent reductions in correlated activity

A. Spike-to-spike coherence between the unit depicted in Figure 2 (which showed individual reductions in variability) and another unit recorded simultaneously from a different electrode. This pair of units exhibited significant reductions in correlated firing at low frequencies (<5 Hz) for attended (red) compared to ignored (blue) trials. Dashed lines indicate the baseline coherence computed after shuffling trials. B. The Pearson correlation computed from the same pair of units using different sized counting windows. Correlations increased in magnitude with longer counting window consistent with the coherent firing being at lower temporal frequencies. Correlations were significantly reduced for attended (red) compared to ignored (blue) trials. As expected, shuffling trials eliminated significant correlations (dashed lines). To compute correlations spike counts were first normalized by subtracting out slow trends in firing rate for each unit using Gaussian smoothing on trial firing rates with a half-width of 5 trials. Scatter plots of normalized spike counts used to compute the correlation are shown below for an attended an ignored case.

Figure 4. Timescales of correlations in noise across population, for attended and unattended stimuli

A. The mean spike-to-spike coherence across 236 pairs for attended (red) and ignored (blue) stimulus trials. The coherence is strongest at low temporal frequencies (<5 Hz) and is significantly reduced by attention. Dashed lines indicate baseline coherence computed from shuffled trials. B. The Pearson correlation computed from the spike counts of 236 pairs as a function of counting window size. Correlations are strong on long timescales, and are reduced for attended (red) compared to unattended (blue) stimuli. C. Scatter plot of attended and unattended correlations are shown split out by monkey subject (green and black) for the 100 ms counting window size (mean values highlighted by black box in panel B). D. Theoretical calculations for the signal to noise ratio as a function of neuronal pool size are shown (analysis methods identical to that of Zohary et al, 1994). For unattended trials (mean correlation of r = 0.068, rate = 10hz), the signal to noise ratio of 100 ms spike counts saturates at an SNR of 3.9 (blue line). A 20% increase in firing rate with attention would result in a 10% increase in the SNR (orange dashed line) whereas the observed reductions in correlation (r = 0.034) with no changes in rate results in a 39% increase.

Figure 5. Time course of attentional modulation

A. Average Fano factors for attended (red line) and unattended (blue line) stimuli (±1 SEM indicated by dashed lines). Yellow vertical lines indicate beginning and end of pause period. The three 400 msec. time periods over which we analyzed correlation and coherence are indicated by dashed vertical lines. The first period (1250–1650 msec after trial onset) began 200 msec before the stimulus paused, so it covered the transient response that occurred as the stimulus swept into the receptive field. The second (1650–2050 msec) and third (2050–2450 msec) windows covered the next two successive 400 msec periods, which together constitute the 800 msec sustained period that is the main focus of analyses in the manuscript. B–D. Correlations computed during each time window, for attended (red line) and unattended stimuli (blue line). E–G. Coherence computed during each time window, for attended (red line) and unattended stimuli (blue line).