Transforming absolute value to categorical choice in primate superior colliculus during value-based decision making

Abstract

Value-based decision making involves choosing from multiple options with different values. Despite extensive studies on value representation in various brain regions, the neural mechanism for how multiple value options are converted to motor actions remains unclear. To study this, we developed a multi-value foraging task with varying menu of items in non-human primates using eye movements that dissociates value and choice, and conducted electrophysiological recording in the midbrain superior colliculus (SC). SC neurons encoded “absolute” value, independent of available options, during late fixation. In addition, SC neurons also represent value threshold, modulated by available options, different from conventional motor threshold. Electrical stimulation of SC neurons biased choices in a manner predicted by the difference between the value representation and the value threshold. These results reveal a neural mechanism directly transforming absolute values to categorical choices within SC, supporting highly efficient value-based decision making critical for real-world economic behaviors.

Flexible control of representational dynamics in a disinhibition-based model of decision making

“…Disinhibition drives a competition between the two R units, resulting in a switch between graded coding of the input ratio to a categorical coding of the largest value ( β = .4 in visualization). Interestingly, a transition of coded information from input values to categorical information has been widely observed in firing rates in decision related regions, such as LIP and superior colliculus, during the delay period of decision making 15, 16, 120 . The point attractor predicted by the circuit under disinhibition (Fig.…”

“…In addition, a transition from graded coding to WTA choice has been widely documented in the decision relevant regions mentioned above. Neural firing rates shows a graded coding of perceptual evidence and reward during the early stage of decision-making and gradually transition to a categorical coding for choice in the late period of decision-making [13][14][15][16][17][18][19]45,120,127 .…”

Neural mechanisms for the localization of externally generated tactile motion

“…Whether this mechanism relies on changes in inhibitory signaling from the SNr or to the activity of local SC interneurons remains an important consideration 6,36,42 . In different behavioral contexts, goal-directed processing may flexibly control the TR to match the expected value of the target stimulus [43][44][45][46] . While visual response habituation has been observed previously in primates and rodents 40,[47][48][49] , our study is the first to demonstrate habituation in the SC supporting somatosensory expectations.…”

“…In this free-form context, habituation of the TR may reflect a central mechanism for ignoring stimuli of diminishing value 29 . In different behavioral contexts, goal-directed processing may flexibly control the TR to match the expected value of the target stimulus [30][31][32][33] . Additional work is needed to determine whether the TR responses described here encode value of environmental cues while decision making.…”

“…Whether this mechanism relies on changes in inhibitory signaling from the SNr or to the activity of local SC interneurons remains an important consideration (Essig et al, 2021; Kaneda et al, 2008; Sooksawate et al, 2011). In different behavioral contexts, goal-directed processing may flexibly control the TR to match the expected value of the target stimulus (Basso and Wurtz, 1998, 1997; Griggs et al, 2018; Zhang et al, 2021). While visual response habituation has been observed previously in primates and rodents (Boehnke et al, 2011; Cynader and Berman, 1972; Drager and Hubel, 1975; K. H. Lee et al, 2020), our study is the first to demonstrate habituation in the SC supporting somatosensory expectations.…”