Orthogonal Representations of Reward Magnitude, Certainty, and Volatility in the Macaque Orbitofrontal Cortex

Abstract

Categorical knowledge about the probabilistic and volatile nature of resource availability can improve foraging strategies, yet we have little understanding of how the brain represents such knowledge. Neurons in the orbitofrontal cortex (OFC) of macaques encode several decision variables (e.g., reward magnitude, probability) that could influence choice behavior. Here we investigated whether OFC neurons also represent two aspects of reward predictability: certainty and volatility. Rhesus monkeys performed a visual stimulus-reward association task in which a set of simple shapes preceded the delivery of reward, and they learned the nature of each shape's reward association along two dimensions. One involved the certainty of a reward outcome; rewards can be either deterministic (and therefore certain) or probabilistic (uncertain). A second dimension reflected the volatility of an outcome; reward schedules can be either stable over time or volatile. During stimulus presentation, the activity of OFC neurons reflected both categorical certainty and categorical volatility, in addition to reward magnitude. These three characteristics were represented orthogonally by three distinct neural populations of similar size. These findings point to a more general role for OFC in processing reward information than one restricted to encoding parametric valuations such as reward magnitude and probability.3 Keywords categorical knowledge, decision making, prefrontal cortex, reward value,

Foraging with the frontal cortex: A cross-species evaluation of reward-guided behavior

“…Consistent with the evidence reviewed above, OFC recordings in monkeys [110] suggest largely orthogonal representations-or single-variable encoding-of reward attributes (i.e., probability, magnitude, volatility). Importantly, the timing of encoding for each of these attributes is simultaneous, suggesting there is parallel encoding of these attributes in OFC [110]. Furthermore, representations of subjective value in OFC are transient and not integrated across the length of time that would be required for decisions [111].…”

Rat Orbitofrontal Ensemble Activity Contains Multiplexed but Dissociable Representations of Value and Task Structure in an Odor Sequence Task

“…This analysis reduced an $1,000-neuron population to a much smaller number of components, and within these, a single component encompassed the bit of information relevant to the value of the current trial, while the remaining components contained the much more detailed information about the sequence of trials in which the value was embedded. While value is often found to co-occur with the encoding of other information in OFC at the level of single units or populations [8, 10, 11, 14-16, 18, 20], this is rarely highlighted (but see [42] and [43]). Showing this co-occurrence clearly and in a complex setting, and showing that the two codes are dissociable has important implications.…”

Rat orbitofrontal ensemble activity contains a multiplexed but value-invariant representation of task structure in an odor sequence task

“…This analysis reduced a ~1000-neuron population to a much smaller number of components, and within these, a single component encompassed the bit of information relevant to the value of the current trial, while the remaining components contained the much more detailed information about the sequence of trials in which the value was embedded. While value is often found to co-occur with encoding of other information in OFC at the level of single units or populations (Howard and Kahnt, 2017;Kennerley et al, 2011;Kennerley et al, 2009;Padoa-Schioppa and Assad, 2006;Roesch et al, 2006;Rudebeck et al, 2013;Thorpe et al, 1983;Tremblay and Schultz, 1999), this is rarely highlighted (but see Farovik et al, 2015;and Yang and Murray, 2018). Showing this co-occurance clearly and in a complex setting, and showing that the two codes are dissociable has important implications.…”