Sensory representations in primary visual cortex are not sufficient for subjective imagery

Abstract

The contemporary definition of mental imagery is characterized by two aspects: a sensory representation resembling, but not resulting from, perception, and an associated subjective experience. Neuroimaging demonstrated imagery-related sensory representations in primary visual cortex (V1) that show striking parallels to perception. However, it remains unclear whether these representations always reflect subjective experience, or they can be dissociated from it. We addressed this question by comparing sensory representations and subjective imagery among visualizers and aphantasics, the latter with an impaired ability to experience imagery. Importantly, to test for the presence of sensory representations independently of the ability to generate imagery on demand we examined both spontaneous and voluntary imagery forms. Using multivariate fMRI, we tested for decodable sensory representations in V1 and subjective visual imagery reports that occurred either spontaneously (during passive listening of evocative sounds) or in response to the instruction to voluntarily generate imagery of the sound content (always while blindfolded inside the scanner). Among aphantasics, V1 decoding of sound content was at chance during voluntary imagery, and lower than in visualizers, but it succeeded during passive listening, despite them reporting no imagery. In contrast, in visualizers, decoding accuracy in V1 was greater in voluntary than spontaneous imagery (while being positively associated with the reported vividness of both imagery types). Finally, for both conditions, decoding in precuneus was successful in visualizers but at chance for aphantasics. Together, our findings show that V1 representations can be dissociated from subjective imagery, while implicating a key role of precuneus in the latter.