PRESERVED TACTILE AND VISUAL VALUE REPRESENTATIONS ACROSS THE PRIMATE STRIATUM AND EXTERNAL GLOBUS PALLIDUS UNDERLYING VALUE-BASED BEHAVIOR

The cortico-basal ganglia circuit exhibits a funneling architecture that conveys information through progressively fewer neurons across successive basal ganglia nuclei which are predominantly GABAergic. Since the putamen (PUT) converges tactile and visual values via bimodal value neurons (Hwang et al., 2024), a critical question arises: how is this information processed in the globus pallidus externus (GPe), a core indirect pathway component? We recorded GPe neuronal activity in two macaque monkeys performing tactile and visual value discrimination tasks. Both monkeys responded faster to good than bad stimuli, confirming their ability to distinguish values across modalities. Among the 134 value-coding neurons, 23% were tactile-selective, 37% visual-selective, and 40% bimodal. Additionally, we analyzed the directionality of value coding in these neuron populations, to examine its functional implications for downstream signaling. We found that a majority of value-coding neurons (n = 90; 67%) increased firing rates for good objects or decreased them for bad objects. Our findings suggest a circuit mechanism, where increased GPe activity for good objects inhibits the globus pallidus internus (GPi) and substantia nigra pars reticulata (SNr), disinhibiting the thalamus to facilitate object choice. Conversely, decreased GPe activity for bad objects disinhibits the GPi/SNr, increasing inhibitory output to the thalamus, leading to object rejection. Our results show that upstream information from PUT is preserved through the indirect pathway, suggesting a circuit-level mechanism by which the GPe guides value-based behavior through disinhibitory control.