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

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.

Optogenetic manipulation of a value-coding pathway from the primate caudate tail facilitates saccadic gaze shift

“…Of particular importance is that the CDt-cdlSNr-SC network conveys the spatial information about good objects. As previously reported, individual neurons in this network have receptive fields at the contralateral periphery [16][17][18]20,26 . It has been found that an SNr neuron projects to a specific site of SC where neurons have visual or oculomotor fields similar to the SNr neuron 35 .…”

“…In the present study, the following two technical approaches were combined in the primate brain: electrophysiological recording of task-related neuronal activity and its optogenetic manipulation in a pathway-selective fashion. The former approach has revealed that numbers of CDt, cdlSNr, and SC neurons represent the stable value of good objects, as previously reported [16][17][18][20][21][22] . The latter approach, on the other hand, has revealed that the CDt-cdlSNr-SC network initiates saccadic eye movements by disinhibition via the two sequential inhibitory pathways (i.e., the CDt-cdlSNr and cdlSNr-SC pathways).…”

“…A series of previous studies have shown that neurons in each structure constituting the CDt-cdlSNr-SC network encode stable values of visual objects in the passive viewing task [16][17][18][20][21][22] . However, it remains to be solved how these neurons convey and transfer the value signals to induce saccadic eye movements.…”

“…On the other hand, neurons in the caudal aspect of the basal ganglia and SC encode the historical value of many visual objects learned through exposure over long time periods [16][17][18][19][20][21] . Such stable value coding is reflected by stable differential responses to good objects (previously associated with larger reward) vs. bad objects (previously associated with smaller or no reward) after objectreward association learning 18,22,23 .…”

Indirect pathway of caudate tail for choosing good objects in periphery

“…These areas have two key features: high-capacity/long-term value memory and peripheral vision. Many neurons along the CDt-circuits (CDt, cvGPe, cdlSNr and SC) sustain their value preference for many objects over a period of months, and discriminate between good and bad objects in peripheral receptive fields (mostly in the contralateral hemisphere) regardless of eccentricity (23,24,26,27). However, their roles in active choice is still unclear, because these neuronal data were based on passive conditions.…”