Fear-Related Signals in the Primary Visual Cortex

Neuronal responses in the primary visual cortex (V1) are driven by simple stimuli, but these stimulus-evoked responses can be markedly modulated by non-sensory factors, such as attention and reward [1], and shaped by perceptual training [2]. In real-life situations, neutral visual stimuli can become emotionally tagged by experience, resulting in altered perceptual abilities to detect and discriminate these stimuli [3-5]. Human imaging [4] and electroencephalography (EEG) studies [6-9] have shown that visual fear learning (the acquisition of aversive emotion associated with a visual stimulus) affects the activities in visual cortical areas as early as in V1. However, it remains elusive as to whether the fear-related activities seen in the early visual cortex have to do with feedback influences from other cortical areas; it is also unclear whether and how the response properties of V1 cells are modified during the fear learning. In the current study, we addressed these issues by recording from V1 of awake monkeys implanted with an array of microelectrodes. We found that responses of V1 neurons were rapidly modified when a given orientation of grating stimulus was repeatedly associated with an aversive stimulus. The output visual signals from V1 cells conveyed, from their response outset, fear-related signals that were specific to the fear-associated grating orientation and visual-field location. The specific fear signals were independent of neurons' orientation preferences and were present even though the fear-associated stimuli were rendered invisible. Our findings suggest a bottom-up mechanism that allows for proactive labeling of visual inputs that are predictive of imminent danger.