Emergence of visually-evoked reward expectation signals in dopamine neurons via the superior colliculus in V1 lesioned monkeys

摘要

To survive and thrive, animals must learn to approach cues in their environment that are likely to lead to a desirable outcome and avoid those that might lead them to harm. A group of brain regions known as the midbrain dopamine system helps many animals to achieve this. Dopamine is the brain’s reward signal. Cues that predict rewards, such as the sight or smell of food, activate midbrain dopamine neurons. However, the details of this process remained unclear. Takakuwa et al. have now examined how visual information that signals reward reaches the midbrain dopamine neurons. The anatomy of the visual system suggests two main possibilities. Information may travel directly from the eyes to an area of the midbrain called the superior colliculus, and then onto the dopamine neurons. Alternatively, information may travel to the midbrain indirectly via a pathway that includes additional processing in the brain’s outer layer, the visual cortex. To distinguish between these routes, Takakuwa et al. studied monkeys in which the indirect pathway via the visual cortex had been damaged. Some people with damage to this pathway have a disorder called blindsight. They are able to detect the movement or location of stimuli, but they cannot consciously see those stimuli. The monkeys with damage to visual cortex were able to learn that an image on a screen predicted the delivery of fruit juice. After repeated trials, the monkeys began to lick the spout dispensing the juice whenever the image appeared, even if no juice was delivered. The monkeys’ midbrain dopamine neurons also sent more signals in response to the images, and showed greater activity when the images predicted large rewards than small ones. Takakuwa et al. next inactivated the superior colliculus with a drug and showed that this prevented both the licking behavior and the increased signaling. Together the findings show that visual information about potential rewards can reach midbrain dopamine neurons via a direct route through the superior colliculus, without needing to pass via the visual cortex. The next step is to determine how and when the visual cortex may get involved in this process to help animals maximize rewards.