Inflammatory pain disrupts the orbitofrontal neuronal activity and risk-assessment performance in a rodent decision-making task

It has been recently described that disruption of the neural mechanisms of emotion-based decision making occurs in both chronic pain patients and in animal models of pain; moreover, it also has been shown that chronic pain causes morphological and functional changes in the prefrontal cortex that may be crucial for this decision-making dysfunction. However, it is not known whether pain alone is capable of altering the neuronal encoding of decision exhibited by prefrontal neurons. We have previously shown that naïve animals have risk-averse performance in the rodent gambling task, whereas chronic pain animals reverse their choice preference and become risk prone. Using this paradigm, we chronically implanted arrays of multielectrodes and recorded from neuronal ensembles in the orbitofrontal cortex of freely moving animals performing 4 sessions of the rodent gambling task: 2 in control conditions and 2 after the onset of inflammatory pain induced by complete Freund's adjuvant injection. Our results show that the instantaneous neuronal firing rate was correlated with the probability of choosing a specific lever in 62.5% of the neurons; however, although in the control sessions 61% of the neurons encoded the reward magnitude, after the pain onset only 16% of the neurons differentiated small from large rewards. Moreover, we found that the fraction of risk-sensitive neurons recorded in each session predicted the overall risk bias of the animal. Our data suggest that orbitofrontal cortex encoding of risk preference is compromised in chronic pain animals.