Journal Article

A hierarchy of timescales explains distinct effects of local inhibition of primary visual cortex and frontal eye fields

Cocchi, Luca, Bell, Peter T, Sale, Martin V, Zalesky, Andrew, Mattingley, Jason B, Nguyen, Vinh T, L Gollo, Leonardo, Breakspear, Michael

2016

Overview

Within the primate visual system, areas at lower levels of the cortical hierarchy process basic visual features, whereas those at higher levels, such as the frontal eye fields (FEF), are thought to modulate sensory processes via feedback connections. Despite these functional exchanges during perception, there is little shared activity between early and late visual regions at rest. How interactions emerge between regions encompassing distinct levels of the visual hierarchy remains unknown. Here we combined neuroimaging, non-invasive cortical stimulation and computational modelling to characterize changes in functional interactions across widespread neural networks before and after local inhibition of primary visual cortex or FEF. We found that stimulation of early visual cortex selectively increased feedforward interactions with FEF and extrastriate visual areas, whereas identical stimulation of the FEF decreased feedback interactions with early visual areas. Computational modelling suggests that these opposing effects reflect a fast-slow timescale hierarchy from sensory to association areas. In humans, the parts of the brain involved in vision are organized into distinct regions that are arranged into a hierarchy. Each of these regions contains neurons that are specialized for a particular role, such as responding to shape, color or motion. To actually ‘see’ an object, these different regions must communicate with each other and exchange information via connections between lower and higher levels of the hierarchy. However, it remains unclear how these connections work. A brain region called the primary visual cortex is the lowest level of the visual cortical hierarchy as it is the first area to receive information from the eye. This region then passes information to higher regions in the hierarchy including the frontal eye fields (FEF), which help to control visual attention and eye movements. In turn, the FEF is thought to provide ‘feedback’ to the primary visual cortex. Cocchi et al. examined how the FEF and primary visual cortex communicate with the rest of the brain by temporarily inhibiting the activity of these regions in human volunteers. The experiments show that inhibiting the primary visual cortex increased communication between this region and higher level visual areas. On the other hand, inhibiting the FEF reduced communication between this region and lower visual areas. Computer simulations revealed that inhibiting particular brain regions alters communication between visual regions by changing the timing of local neural activity. In the simulations, inhibiting the primary visual cortex slows down neural activity in that region, leading to better communication with higher regions, which already operate on slower timescales. By contrast, inhibition of the FEF reduces its influence on lower visual regions by increasing the difference in timescales of neural activity between these regions. The next step is to determine whether similar mechanisms regulate changes in the activity of neural networks outside of the visual system.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Adult / Computational Biology / Computational neuroscience / connectivity / Cortex (frontal) / Cortex (somatosensory) / cortical hierarchy / Eye / Feedback / Female / Frontal Lobe - physiology / functional magnetic resonance imaging (fMRI) / Healthy Volunteers / Humans / Male / modelling / Models, Neurological / Neural circuitry / Neural Inhibition / Neural networks / Neuroimaging / Neuroscience / Physiological aspects / Simulation / temporal hierarchy / Time Factors / Transcranial Magnetic Stimulation / transcranial magnetic stimulation (TMS) / Visual cortex / Visual Cortex - physiology / Visual stimuli / Visual system / Young Adult