Value-based search efficiency is encoded in substantia nigra reticulata firing rate, spiking irregularity and local field potential

Recent results show that valuable objects can pop-out in visual search yet its neural mechanisms remain unexplored. Given the role of substantia nigra reticulata (SNr) in object value memory and control of gaze, we recorded its single unit activity while male macaque monkeys engaged in efficient or inefficient search for a valuable target object among low-value objects. Results showed that efficient search was concurrent with stronger inhibition and higher spiking irregularity in target present (TP) compared to target absent (TA) trials in SNr. Importantly, the firing rate differentiation of TP and TA trials happened within ∼100ms of display onset and its magnitude was significantly correlated with the search times and slopes (aka search efficiency). Time-frequency analyses of local field potential (LFP) after display onset revealed significant modulations of gamma band power with search efficiency. The greater reduction of SNr firing in TP trials in efficient search can create a stronger disinhibition of downstream superior colliculus which in turn can facilitate saccade to obtain valuable targets in competitive environments. Significant statement Most times we have to find a few relevant or highly valued objects among many objects that surround us. When our target objects are not distinct from their surroundings based on low-level features, searching for them becomes tedious and slow. Nevertheless, recent findings show that valuable objects can be found efficiently and fast if they have been repeatedly paired with reward. Our results show that the rate and pattern of spiking as well as local voltage fluctuations in the basal ganglia output which is known to control attention and saccade correlate with such value-driven search efficiency. Thus, in addition to reward learning, basal ganglia can have a role in skillful interactions with and rapid detection of rewarding objects.