Attention Selects Informative Neural Populations in Human V1

Abstract

In a neural population driven by a simple grating stimulus, different sub-populations are maximally informative about changes to the grating’s orientation and contrast. In theory, observers should attend to the optimal subpopulation when switching between orientation and contrast discrimination tasks. Here we used source-imaged, steady-state visual evoked potentials (SSVEPs) and visual psychophysics, to determine whether this is the case. Observers fixated centrally while static targets were presented bilaterally along with a cue indicating task type (contrast or orientation modulation detection) and task location (left or right). Changes in neuronal activity were measured by quantifying frequency-tagged responses from flickering ‘reporter’ gratings surrounding the targets. To determine the orientating tuning of attentionally-modulated neurons, we measured responses for three different probe-reporter angles: 0, 20 and 45°. We estimated frequency-tagged cortical activity using a minimum norm inverse procedure combined with realistic MR-derived head models and retinotopically-mapped visual areas. Estimates of neural activity from regions of interest centered on V1 showed that attention to a spatial location clearly increased the amplitude of the neural response in that location. More importantly, the pattern of modulation depended on the task. For orientation discrimination, attentional modulation showed a sharp peak in the population tuned 20° from the target orientation, whereas for contrast discrimination the enhancement was more broadly tuned. Similar tuning functions for orientation and contrast discrimination were obtained from psychophysical adaptation studies. These findings indicate that humans attend selectively to the most informative neural population and that these populations change depending on the nature of the task.

Attention Modifies Spatial Resolution According to Task Demands

“…Consistent with the finding that humans can selectively attend to the most informative neuronal population (Verghese, Kim, & Wade, 2012), our results portray endogenous attention as an adaptive mechanism that can swiftly modify resolution according to task demands. Whether resolution becomes finer or coarser with attention depends on the resolution constraints–that is, the relation between the scale of the relevant information and the visual system's resolution at that location.…”

A review of the mechanisms by which attentional feedback shapes visual selectivity

“…In addition, this enhancement of feature-selective responses has been found to occur non-selectively across space (Saenz et al 2002; Sàenz et al 2003; Serences and Boynton 2007; Jehee et al 2011), which is consistent with physiological studies showing effects of feature-based attention spreading across the visual field (Treue and Martínez Trujillo 1999). Using similar decoding techniques, others have found a sharpening of the population response with feature-based attention (Serences et al 2009a), and changes in population activity consistent with the notion that attentional feedback targets the most informative neurons in the current behavioral task (Scolari and Serences 2009; Scolari and Serences 2010; Verghese et al 2012). Consistent with this, when attentional modulation is spread thin across multiple items, the selectivity of population responses has been shown to be broader than when the focus is on just one item (Anderson et al 2013).…”

Encoding of graded changes in spatial specificity of prior cues in human visual cortex

“…Indeed, sensory enhancement in the form of sharpened orientation tuning has been reported for orientation discrimination when prior information is provided in humans (Anderson et al 2013;Jehee et al 2011;Kok et al 2012), though not in monkeys (McAdams and Maunsell 1999). Contrast discrimination may benefit more from summation across many neurons all with monotonically increasing contrast responses (Verghese et al 2012), and therefore behavioral performance may tend to be initially based on a less selective sampling of neurons. Efficient selection then, particularly in the presence of multiple possible targets, may be a more critical neural mechanism for improving behavioral performance.…”

“…Moreover, the particular task performed may influence whether sensory enhancement or efficient selection plays a dominant role. In orientation discrimination, for example, neurons whose orientation tuning provides the most amount of information relevant to discrimination may already be more strongly weighted than others (Jazayeri and Movshon 2007;Purushothaman and Bradley 2005;Serences 2009, 2010;Scolari et al 2012;Seung and Sompolinsky 1993;Verghese et al 2012) so that additional selection through attentional selection may be less effective. Indeed, sensory enhancement in the form of sharpened orientation tuning has been reported for orientation discrimination when prior information is provided in humans (Anderson et al 2013;Jehee et al 2011;Kok et al 2012), though not in monkeys (McAdams and Maunsell 1999).…”