Single-Neuron Responses in the Human Nucleus Accumbens during a Financial Decision-Making Task

Abstract

Linking values to actions and evaluating expectations relative to outcomes are both central to reinforcement learning and are thought to underlie financial decision-making. However, neurophysiology studies of these processes in humans remain limited. Here, we recorded the activity of single human nucleus accumbens neurons while subjects performed a gambling task. We show that the nucleus accumbens encodes two signals related to subject behavior. First, we find that under relatively predictable conditions single neuronal activity predicts future financial decisions on a trial-by-trial basis. Interestingly, we show that this activity continues to predict decisions even under conditions of uncertainty (e.g. when the probability of winning and losing is 50/50 and no particular financial choice predicts a rewarding outcome). Furthermore, we find that this activity occurs, on average, two seconds before the subjects physically manifests their decision. Second, we find that the nucleus accumbens encodes the difference between expected and realized outcomes, consistent with a prediction error signal. We show this activity occurs immediately after the subject has realized the outcome of the trial and is present on both the individual and population neuron level. These results provide human single neuronal evidence that the nucleus accumbens is integral in making financial decisions.

The Nucleus Accumbens: An Interface Between Cognition, Emotion, and Action

“…As mentioned above, it is difficult to disentangle how much of the fMRI BOLD response associated with choice behavior is attributable to the activity either of intrinsic NAc neurons or of inputs arising from frontal and temporal lobe regions. However, a study by Patel et al (2012) employed electrophysiological recordings from individual NAc neurons in humans. Subjects played a gambling task resembling the card game "War," wherein they drew cards of different numerical values from a deck and had to wager either $20 or $5 that their card would be higher than the one drawn by a computer opponent.…”

Intracranial Applications of Magnetic Resonance-guided Focused Ultrasound

“…Unlike GKRS, MRgFUS does not use ionizing radiation, thus permitting multiple treatments, if necessary, without concern for cumulative radiation exposure. With GKRS there is also concern regarding variable biological responses to radiation and the development of secondary malignancy [85], the risk of which has been estimated to be 0.04-0.10 % [86,87]. Arguably the most important putative advantage of MRgFUS is that the effect of treatment is immediate, rather than delayed, as is the case with GKRS [46,85,88].…”

Studying task-related activity of individual neurons in the human brain

“…For these reasons, we recommend simple, well-balanced tasks with sufficient repetition. There are many available references for examples of behavioral tasks 16,[18][19][20]24 . Placing fibrin glue (Tisseel, or other similar biological material) within the burr hole helps to reduce CSF loss and to dampen brain pulsations, thereby improving recording stability, especially for cortical recordings.…”

“…6). In a different study exploring financial decision making, we were able to perform trial-by-trial analyses correlating neurophysiological signals with upcoming behavior 19 . By using a receiver operating characteristic (ROC) analysis, we showed on a trial-by-trial basis that neurons in the nucleus accumbens encoded upcoming decisions well in advance of the physical manifestation of that behavioral choice (Fig.…”

“…Previous studies have investigated the role of the basal ganglia in motor planning 16 and of the substantia nigra in reward expectation 17 . We recently demonstrated the function of the cingulate cortex in processing cognitive interference 18 , of the nucleus accumbens in financial decision making 19 and of the dorsolateral prefrontal cortex in abstract rule encoding 20 .…”