Perceptual decision making is a complex process that requires multiple computations, including the accumulation of sensory evidence and an ongoing evaluation of the accumulation process to use for prediction and adjustment. Implementing these computations likely involves interactions among many brain regions. For perceptual decisions linked to oculomotor actions, neural correlates of sensory evidence accumulation have been identified in several cortical areas, including the frontal eye field and lateral intraparietal area, and one of their direct, subcortical targets, the superior colliculus. These structures are also connected indirectly, via the basal ganglia. The basal ganglia pathway has been theorized to contribute to perceptual decision making, but the nature of this contribution has yet to be examined directly. Here we show that in monkeys performing a reaction-time visual motion direction-discrimination task, neurons in a primary input structure of the basal ganglia, the caudate nucleus, encode three aspects of decision making: evidence accumulation, evaluation, and choice biases. These results indicate that the basal ganglia pathway can provide important signals to influence and assess perceptual decisions that guide oculomotor behavior.

Perceptual decision making requires a complex set of computations to implement, evaluate, and adjust the conversion of sensory input into a categorical judgment. Little is known about how the specific underlying computations are distributed across and within different brain regions. Using a reaction-time (RT) motion direction-discrimination task, we show that a unique combination of decision-related signals is represented in monkey frontal eye field (FEF). Some responses were modulated by choice, motion strength, and RT, consistent with a temporal accumulation of sensory evidence. These responses converged to a threshold level prior to behavioral responses, reflecting decision commitment. Other responses continued to be modulated by motion strength even after decision commitment, possibly providing a memory trace to help evaluate and adjust the decision process with respect to rewarding outcomes. Both response types were encoded by FEF neurons with both narrow- and broad-spike waveforms, presumably corresponding to inhibitory interneurons and excitatory pyramidal neurons, respectively, and with diverse visual, visuomotor, and motor properties, albeit with different frequencies. Thus, neurons throughout FEF appear to make multiple contributions to decision making that only partially overlap with contributions from other brain regions. These results help to constrain how networks of brain regions interact to generate perceptual decisions.

Perceptual decision-making is a computationally demanding process that requires the brain to interpret incoming sensory information in the context of goals, expectations, preferences, and other factors. These integrative processes engage much of cortex but also require contributions from subcortical structures to affect behavior. Here we summarize recent evidence supporting specific computational roles of the basal ganglia in perceptual decision-making. These roles likely share common mechanisms with the basal ganglia’s other, more well-established functions in motor control, learning, and other aspects of cognition and thus can provide insights into the general roles of this important subcortical network in higher brain function.

The frontal eye field (FEF) influences saccade generation via direct projections to the superior colliculus and an indirect pathway through the basal ganglia. To test whether different reward information is represented in the FEF and the basal ganglia, we recorded from the FEF and the caudate nucleus in monkeys performing an asymmetrically rewarded memory-guided saccade task. A peripheral cue at one of two opposing positions was flashed briefly to indicate the saccade target. In a given block, one position was associated with big reward and the other with small reward. Big-reward position was alternated between blocks. In this task, the FEF and caudate displayed similar prevalence of neuronal activity before cue onset that was larger in blocks with specific big reward-cue position associations. They also exhibit comparable reward modulation of visual responses that were spatially selective. In contrast, visual responses that were specific to expected reward size, instead of spatial locations, were commonly observed in caudate but rarely seen in the FEF. Thus, both the FEF and basal ganglia may contribute to reward bias in saccade generation, with the FEF providing spatially relevant reward information and the basal ganglia providing additional reward-specific information.