Spiking Suppression Precedes Cued Attentional Enhancement of Neural Responses in Primary Visual Cortex

Abstract

Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naïve subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses.

Figure 1.

Experimental paradigm and psychophysical data. (a) Modified Posner spatial attention task. Animals are rewarded for correctly indicating a contrast change in one of the peripheral gratings via a lever press or correctly withholding a response in the absence of a change on catch trials. The cue presented at fixation earlier in the trial predicts the location of stimulus change with 80–90% validity. (b) Behavioral performance. Plots show contrast sensitivity in d’ as a function of contrast decrements across “valid cue” (red) and “invalid cue” (gray) trials for each monkey average over behavioral testing days (point size scales with the number of sessions included in average). Curves are logistic fits. (c) Average reaction time of each monkey to the contrast decrement across valid cue (red) and invalid cue (gray) trials. Error bars represent standard error of the mean (SEM). See Supplementary Table 1 for detailed statistical analysis of behavioral data. (d) Relative locations of fixation dot (black), foveal cue (gray), and mapped receptive fields (green dots for B, blue for E, red for naïve subject). For visualization purposes, receptive field diameters (solid lines) were estimated from the mapped receptive field (RF) centers using an estimate of cortical magnification (diameter = 0.21*eccentricity (Freeman and Simoncelli 2011)), and fitted with a Gaussian gradient. (e) Stability of fixation. Horizontal (top) and vertical (bottom) gaze position relative to fixation for the ±250 ms surrounding foveal cue onset (n = 25 trials, monkey E).

Figure 2.

V1 spiking responses. (a) Time course of analog MUA for unattended (gray) and attended (red) stimulus presentations inside the receptive field, averaged across all penetrations (N = 70, monkeys E and B) and V1 multiunits (n = 993, monkeys E and B). MUA is expressed in percent change from the pre-stimulus baseline. Stimulus onset occurred at t = 0 s (vertical solid line), which preceded the attentional cue by 800 ms (vertical dashed line). Ordinate is truncated for display purposes. (b) Time course of MUA following cue onset. The naïve monkey (blue line: n = 273 multiunits across N = 18 penetrations) shows no decrease from baseline following cue onset. Both trained monkeys (purple line: n = 351 V1 multiunits across N = 25 penetrations in E; green: n = 642 multiunits across N = 45 penetrations in B) exhibited a decrease in MUA immediately following cue onset (vertical black arrow) even after excluding trials with microsaccades immediately before or after the cue (see Methods).

Figure 3.

Laminar spiking profiles. (a–c) Average analog MUA across V1 layers for each monkey E, monkey B, and the naïve monkey. The stimulus array and the foveal cue where shown at each t = 0 s and t = 0.8 s respectively. Black vertical arrows mark spiking suppression exclusive to trained subjects. The naïve monkey was ignorant to the task-relevance of the cue. (d) Latency of responses following each the stimulus onset (gray) and the foveal cue onset (black) in trained monkeys E and B. Solid line represents the median across all penetrations and dashed lines represent 95% confidence limits on the median. Note the differences in absolute response latency between the stimulus-evoked response and the cue-evoked response as well as inverse laminar pattern between conditions. (e) Spatial profile of suppression. The main stimulus array consisted of 4 identical, isoeccentric gratings. The receptive fields of the neurons under study always coincided with the grating in the lower right quadrant. On a given trial, the foveal cue could point to any of the 4 gratings in the array. For each monkey E and monkey B, average MUA following cue onset (t = 0.8 s) is plotted for each cue direction (blue = low right quadrant, purple = upper right quadrant, green = upper left quadrant, orange = lower left quadrant; see Supplementary Fig. 6 for schematic).

Figure 4.

Laminar profile of cue-induced spiking suppression (discretized MUA) compared with attention-related response gain. For each laminar recording location (vertical axis plots cortical depth, with each bar’s spacing = 100 μm ± 50 μm), in each monkey (left vs. right), metrics of each cue-induced suppression (mean decrease in spiking 100–200 ms from cue onset) and attention-related response gain (mean difference between attended and unattended condition 300–1600 ms following cue onset) are plotted. Error bars are SEM across penetrations (N = 45 for monkey B, N = 25 for monkey E).

Figure 5.

Current-source density (CSD) analysis. (a) Laminar time course of CSD following cue onset expressed as z-score across penetrations for the 2 trained monkeys (N = 70). Bar plot to the right shows the mean CSD amplitude across the cortical depth spanned by the bar’s height in units of nanoamperes per mm³. Error bars are SEM across recording sessions. CSD activity differs significantly across the L4C/L5 border (Monkey B: t(74) = −8.26, P < 0.001; Monkey E: t(38) = −4.46, P < 0.001), with a current sink occurring in the deep layers and a current source in the middle layers. (b) Laminar time course of CSD following stimulus onset in the trained subjects (N = 70 penetrations, 2 monkeys). All conventions and units as in panel a. CSD activity differs significantly across the L4C/L5 border (Monkey B: t(74) = 14.38, P < 0.001; Monkey E: t(38) = 8.85, P < 0.001), with a current sink occurring in the middle layers and a current source in the deep layers, consistent with previous reports. The pronounced current sink marks the granular layer (L4C), the main locus of activation from LGN. (c) Laminar time course of CSD activity following cue onset in the naïve monkey (N = 15 penetrations). There was no significant difference in CSD activity the across the L4C/L5 border (t(28) = 0.66, P = 0.517). All conventions and units as in panel a. (d) Laminar time course of CSD following stimulus onset across penetrations in a naïve monkey (N = 15 penetrations). CSD activity differs significantly across the L4C/L5 border (t(28) = 6.45, P < 0.001), with a pronounced current sink in granular L4C. All conventions and units as in panel a.