Abstract
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.
Highlights
The superior colliculus (SC) is an important brain region of mammals that allows them to precisely control their gaze direction and orient toward relevant and salient objects in their surrounding world
We explored this question by testing whether SC neurons respond differently to objects previously associated with different amounts of reward value
To test whether long-term reward history of visual objects affected the visual response of SC neurons, we performed experiments in three phases in this study
Summary
The superior colliculus (SC) is an important brain region of mammals that allows them to precisely control their gaze direction and orient toward relevant and salient objects in their surrounding world These functions are facilitated by the SC’s involvement with visual spatial attention and its role in generating a retinotopic priority map for target selection (Fecteau and Munoz, 2006; Krauzlis et al, 2013; Wolf et al, 2015; Crapse et al, 2018). This suggests that SC plays an important role in action selection and attention by helping choose what sensory information is most relevant to future actions To help form this priority map, signals from many cortical and subcortical regions converge on the SC and modulate the activity of its neurons (see review Krauzlis et al, 2013)
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