A potential cortical precursor of visual word form recognition in untrained monkeys

Skilled human readers can readily recognize written letters and letter strings. This domain of visual recognition, known as orthographic processing, is foundational to human reading, but it is unclear how it is supported by neural populations in the human brain. Behavioral research has shown that non-human primates (baboons) can learn to distinguish written English words from pseudo-words (lexical decision), successfully generalize that behavior to novel strings, and exhibit behavioral error patterns that are consistent with humans. Thus, non-human primate models, while not capturing the entirety of human reading abilities, may provide a unique opportunity to investigate the neuronal mechanisms underlying orthographic processing. Here, we investigated the neuronal representation of letters and letter strings in the ventral visual stream of naive macaque monkeys, and asked to what extent these representations could support visual word recognition. We recorded the activity of hundreds of neurons at the top two levels of the ventral visual form processing pathway (V4 and IT) while monkeys passively viewed images of letters, English words, and non-word letter strings. Linear decoders were used to probe whether those neural responses could support a battery of orthographic processing tasks such as invariant letter identification and lexical decision. We found that IT-based decoders achieved baboon-level performance on these tasks, with a pattern of errors highly correlated to the previously reported primate behavior. This capacity to support orthographic processing tasks was also present in the high-layer units of state-of-the-art artificial neural network models of the ventral stream, but not in the low-layer representations of those models. Taken together, these results show that the IT cortex of untrained monkeys contains a reservoir of precursor features from which downstream brain regions could, with some supervised instruction, learn to support the visual recognition of written words. This suggests that the acquisition of reading in humans did not require a full rebuild of visual processing, but rather the recycling of a brain network evolved for other visual functions.