Top-Down Modulation of Lateral Interactions in Visual Cortex

Abstract

The primary visual cortex (V1) changes its computation according to the perceptual task being performed. We propose that this cognitive modulation results from gating of V1 intrinsic connections. To test this idea, using behavioral paradigms that engage top-down modulation of V1 contextual interactions, we recorded from chronically implanted electrode arrays in macaques. We observed task-dependent changes in interactions between V1 sites measured both by correlation between spike trains and by coherence between local field potentials (LFP-LFP coherence). The direction of the changes in aggregate activity (LFP) depended on perceptual strategy: perceptual grouping increased LFP coherence between sites crucial for the task, while perceptual segregation lowered the LFP coherence. Using spiking activity as a measure, we found that the behaviorally-driven changes in correlation structure between neurons dramatically increased the stimulus-related information that they convey; this additional increase in encoded information at the level of neuronal ensembles equals that obtained from task-driven reconfigurations of neural tuning curves. The improvements in information encoding were strongest for stimuli with greatest discrimination difficulty.

On the functions, mechanisms, and malfunctions of intracortical contextual modulation

“…These effects were greatest when the feedforward drive was present but weak. However, Ramalingam et al (2013) also found that V1 cells have higher firing rates when the element to which they were selectively sensitive was part of a contour. Amplification increased with contour length, and occurred with a latency of about 100 ms following stimulus onset.…”

“…In some conditions the amplifying effects of attention occur with latencies of more than 100 msec (e.g. Li, Piech and Gilbert, 2006;Roelfsema, Lamme, and Spekreijse, 1998;Bisley and Goldberg, 2006), but when attention can be oriented appropriately prior to stimulus onset its effects can be observed in LFPs prior to stimulus onset (Ramalingam et al, 2013). They can then affect the very first spike (Gilbert and Sigman, 2007).…”

“…In addition to amplifying responses, attention can also facilitate contextual effects within V1 (e.g. Ito and Gilbert, 1999), particularly when stimuli are ambiguous (Ramalingam et al, 2013).…”

“…More recent results suggest that amplification and synchronization may both be involved in grouping. For example, Ramalingam et al (2013) found that in awake behaving macaques perceptual grouping increased the synchronization of LFPs in V1, whereas perceptual segregation lowered synchronization. These effects were greatest when the feedforward drive was present but weak.…”

“…Much has now been learned about facilitation by flankers, including evidence that it involves amplifying modulation (Chen and Tyler, 2008;Huang, Hess and Dakin, 2006;Maehara, Huang and Hess, 2010), can be cancelled by non-collinear flanks (Solomon and Morgan, 2000); depends upon input from other parts of the adjacent surround (Mareschal and Clifford, 2013), and is itself modulated by attention (Ramalingam et al, 2013). Psychophysical studies show that detection is improved when the flankers precede the target, or are presented simultaneously with it, but not when the target precedes the flankers (Polat and Sagi, 2006).…”