How do the blind 'see'? The role of spontaneous brain activity in self-generated perception.

Avital Hahamy,Boris Rosin,Marlene Behrmann,Rafael Malach,Meytal Wilf

doi:10.1093/brain/awaa384

Abstract

Spontaneous activity of the human brain has been well documented, but little is known about the functional role of this ubiquitous neural phenomenon. It has previously been hypothesized that spontaneous brain activity underlies unprompted (internally generated) behaviour. We tested whether spontaneous brain activity might underlie internally-generated vision by studying the cortical visual system of five blind/visually-impaired individuals who experience vivid visual hallucinations (Charles Bonnet syndrome). Neural populations in the visual system of these individuals are deprived of external input, which may lead to their hyper-sensitization to spontaneous activity fluctuations. To test whether these spontaneous fluctuations can subserve visual hallucinations, the functional MRI brain activity of participants with Charles Bonnet syndrome obtained while they reported their hallucinations (spontaneous internally-generated vision) was compared to the: (i) brain activity evoked by veridical vision (externally-triggered vision) in sighted controls who were presented with a visual simulation of the hallucinatory streams; and (ii) brain activity of non-hallucinating blind controls during visual imagery (cued internally-generated vision). All conditions showed activity spanning large portions of the visual system. However, only the hallucination condition in the Charles Bonnet syndrome participants demonstrated unique temporal dynamics, characterized by a slow build-up of neural activity prior to the reported onset of hallucinations. This build-up was most pronounced in early visual cortex and then decayed along the visual hierarchy. These results suggest that, in the absence of external visual input, a build-up of spontaneous fluctuations in early visual cortex may activate the visual hierarchy, thereby triggering the experience of vision.

Highlights

During rest and independent of any external stimulation, the brain evinces activation in a spontaneous manner (‘resting state’ activity) (Arieli et al, 1995; Nir et al, 2006; Fox and Raichle, 2007; Raichle, 2009; Harmelech and Malach, 2013; Moutard et al, 2015)
Unlike other types of visual experiences, visual hallucinations are related to a spontaneous build-up of neural activity, which is most pronounced in early visual cortex, and decays along the visual hierarchy
Our findings propose a network view of visual hallucinations in Charles Bonnet syndrome (CBS), under which a slow build-up of spontaneous neural activity in early visual regions may bring about a perception of vision by triggering a cascade of activity throughout the visual system

Summary

Introduction

During rest and independent of any external stimulation, the brain evinces activation in a spontaneous manner (‘resting state’ activity) (Arieli et al, 1995; Nir et al, 2006; Fox and Raichle, 2007; Raichle, 2009; Harmelech and Malach, 2013; Moutard et al, 2015). It has previously been proposed that a slow build-up of spontaneous activity can initiate unprompted (spontaneous) behaviour (Schurger et al, 2012; Moutard et al, 2015) This phenomenon has been classically observed in the readiness potential during decisions to move (Kornhuber and Deecke, 1965; Libet et al, 1983; Libet, 1985; Soon et al, 2008; Fried et al, 2011), but has been observed during other cognitive tasks (Gelbard-Sagiv et al, 2008, 2018; Norman et al, 2019; Broday-Dvir and Malach, 2020). As neurons deprived of external inputs demonstrate enhanced spontaneous brain activity (Echlin et al, 1952; Loeser and Ward, 1967; Segal and Furshpan, 1990), it has been theorized that spontaneous activity in the deprived visual cortex of individuals with CBS may subserve hallucinations (Cogan, 1973; Burke, 2002; Plummer et al, 2007; Reichert et al, 2013)

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