Temporal–prefrontal cortical network for discrimination of valuable objects in long-term memory

Significance Animals, including humans, are surrounded by many objects, only some of which are valuable. To survive, it is critical to efficiently discriminate valuable objects, particularly those that are only occasionally or seasonally available. Here, we use fMRI to show that, in macaques, a network consisting of areas in the temporal and prefrontal cortex and their associated subcortical structures maintained value memories for a large number of objects. This memory representation lasted for many months after the objects were last seen and accordingly the monkeys were able to find valuable objects efficiently. We postulate that this temporal–prefrontal circuit is critical for drawing on learned value memory to guide goal-oriented behavior toward certain objects. Remembering and discriminating objects based on their previously learned values are essential for goal-directed behaviors. While the cerebral cortex is known to contribute to object recognition, surprisingly little is known about its role in retaining long-term object–value associations. To address this question, we trained macaques to arbitrarily associate small or large rewards with many random fractal objects (>100) and then used fMRI to study the long-term retention of value-based response selectivity across the brain. We found a pronounced long-term value memory in core subregions of temporal and prefrontal cortex where, several months after training, fractals previously associated with high reward (“good” stimuli) elicited elevated fMRI responses compared with those associated with low reward (“bad” stimuli). Similar long-term value-based modulation was also observed in subregions of the striatum, amygdala, and claustrum, but not in the hippocampus. The value-modulated temporal–prefrontal subregions showed strong resting-state functional connectivity to each other. Moreover, for areas outside this core, the magnitude of long-term value responses was predicted by the strength of resting-state functional connectivity to the core subregions. In separate testing, free-viewing gaze behavior indicated that the monkeys retained stable long-term memory of object value. These results suggest an implicit and high-capacity memory mechanism in the temporal–prefrontal circuitry and its associated subcortical regions for long-term retention of object-value memories that can guide value-oriented behavior.