Visual Neurons in the Superior Colliculus Discriminate Many Objects by Their Historical Values

Whitney S. Griggs, Hidetoshi Amita, Atul Gopal, Okihide Hikosaka

The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal toward distinct visual events. Visually responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (>10 days) to saccade to multiple fractal objects, half of which were consistently associated with large rewards while other half were associated with small rewards. This created historically high-valued ('good') and low-valued ('bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (>1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior.