V1 isn’t just for seeing

The latest issue of Neuron has a fantastic article on visual attention from Maurizio Corbetta’s group at Washington University in St. Louis. In it, Jack and colleagues report finding a novel signal in V1 independent of other, relatively well-characterized signals.

V1 is the primary visual cortex–essentially, the first cortical stop for incoming visual information. The traditional view used to be that, because of their position at the bottom of the information-processing hierarchy, neurons in V1 respond only to very simple configurations of light patterns (e.g., specific spatial orientations or frequencies). That view is increasingly being challenged by anatomical data indicating that V1 receives projections from a variety of other cortical areas and functional data showing that V1 neurons respond to a variety of seemingly high-level properties .

For example, Shuler & Bear recently demonstrated that neurons in rat visual cortex anticipate the onset of reward, showing a ‘learning’ profile much like that of dopamine neurons in much more anterior regions (i.e., closer to the front of the brain). In humans, neuroimaging studies reliably observe a top-down effect of spatial attention on visual cortex activation: when you expect a stimulus to appear in a particular location, activation in much of visual cortex (including V1) increases. What’s striking about this effect is that it’s endogenous (i.e., it’s produced by the brain and not by sensory information). The amplification occurs irrespective of whether a stimulus actually appears on-screen or not; what matters is whether people are visually attending to a spatial location. Moreover, the effect is spatially specific. V1 is highly retinotopic, meaning that it preserves the spatial structure of light hitting the retina quite well. By ‘stretching’ V1 out and visualizing it as a flat surface (normally it wraps around the banks of the occipital sulcus), researchers can actually pinpoint the location of stimuli in the environment based on the neural response. It turns out that the top-down modulation of V1 is strongest in the area of cortex that corresponds to the attended location in space.

The fact that attention is capable of modulating even the earliest reaches of visual cortex is pretty remarkable. Still, it’s at least intuitive that paying attention to a particular location would facilitate visual processing there (much of the early neuroimaging research on spatial attention was motivated by Posner and colleagues’ behavioral work demonstrating the existence of large facilitation effects). And it’s not exclusive to V1 by any means: the higher up in the visual hierarchy one goes, the stronger the facilitation effect gets.

The finding Jack et al. report in Neuron is just as intriguing, but much less intuitive. Essentially, they’ve discovered a signal in V1 that’s tied specifically to what they refer to as ‘task structure’. That is, the signal is produced whenever a task-relevant event occurs–e.g., a motor response. How did they identify the signal? Here’s what their first experiment looked like:

As you can see, there are two conditions in the task: immediate response and delayed response. In both cases, a checkerboard pattern is presented in 50% of trials and no stimulus s presented in the other 50%. However, in the immediate response condition, participants respond almost as soon as the stimulus period is over (their task is simply to judge whether the checkerboard was present or not), whereas in the delayed response condition there’s an 8 second delay before the response. That separation allowed the authors to compare the timecourse of visual cortex activation across the two conditions to detect any changes in signal. Here’s what they found:

The solid lines in this figure represent trials when the stimulus was actually presented; the dashed lines represent trials where there was no change in the visual display. Clearly, none of the effects depend on the actual presence of the stimuli, so I won’t say anything else about that. (Ignore the line colors for the moment; I’ll get to that in a second).

The figure pretty much tells the story. The left panel shows the V1 response when the subject’s motor response immediately follows the expected stimulus. As you can see, there’s only one peak, probably because the two events (stimulus and response) are so close together than fMRI isn’t able to tease them apart. Presumably, this lack of temporal resolution is also why (amazingly!) no one else had detected this effect before (people don’t t normally use 10 second trials just for the hell of it).

In contrast, if you look at the right panel, you can clearly see two distinct peaks of activation. The first is locked to the stimulus, the second to the motor response. The remarkable aspect of this finding is that there’s no change in visual display when the motor response occurs. The response period is cued by an auditory tone, so the second peak doesn’t reflect anything that’s happening on screen.

The fun doesn’t stop there. In addition to the temporal dissociation between the two V1 signals, Jack et al. also found two more ways in which the signals differed. One is apparent if you look at the colors in the right panel. The blue lines represent foveated stimuli (i.e., stimuli that are presented right in the center of the display, where vision is most acute) and the red lines represent stimuli presented in the periphery. What you can see is that the attention-induced V1 response (the first peak) is, not surprisingly, largest in the location where the subject expects the stimulus to appear. In contrast, the response-locked second peak is stronger in the more eccentric regions of V1 corresponding to peripheral spatial locations. In subsequent experiments, Jack et al. show that these effects are consistent: the stimulus-locked signal occurs wherever subjects expect the stimulus to appear, and the response-locked signal is always stronger in the periphery.

A second dissociation isn’t apparent in the figure above, because I removed the other panels (showing the timecourses in other areas of visual cortex) for simplicity’s sake. But the general finding is that, whereas the stimulus-locked signal is stronger in higher visual regions, the response-locked effect occurs almost exclusively in V1. That’s a pretty dramatic result in and of itself, since it suggests the latter signal is driven by bottom-up influences, and isn’t attentional.

The rest of the paper (including 5 other experiments) basically consists of a very meticulous attempt to rule out alternative sources of the response-locked V1 signal. I won’t go into detail, but here’s a short list of what Jack et al. show: (a) the signal isn’t just locked to overt motor responses, since it occurs even on ‘no-go’ trials when subjects aren’t supposed to respond; (b) the signal isn’t due to the auditory tone signaling the response phase (there are known projections from auditory cortex to V1, so this is a potential confound), because it occurs even when subjects count silently to themselves for 8 seconds before making self-generated responses; and (c) the signal isn’t due to blinks or eye movements, because it holds even after controlling for these factors. Suffice it to say that the effect appears to be highly reliable, doesn’t depend on obvious (and some not so obvious) confounds, and is independent of the previously identified top-down signal throughout visual cortex. In short, methodologically, the paper seems impeccable.

Of course, to many people, the question is: what does this signal mean? Here, Jack et al. don’t have very much to say. But then, it’s hard to blame them: as they observe themselves, what they’ve identified is, paradoxically, a signal in the earliest and most topographically organized part of visual cortex that’s nonperceptual and spatially diffuse. One possibility the authors reject is the notion that the signal might reflect a generic process such as arousal. They note that regions outside of visual cortex don’t show the same effect, and that the signal’s intensity doesn’t seem to track arousal-related variables such as task difficulty. Instead, Jack et al.’s major positive suggestion is that the novel V1 signal could potentially demarcate event boundaries, acting as a relatively general gating signal that helps the cognitive system transition between discrete states. It’s a pretty speculative idea, but the dynamics of the signal are so counter-intuitive that it’s hard to think of plausible alternatives. Given the impact that the study will probably have, odds are it won’t be long before a flurry of follow-up articles come along to hopefully provide more insight.