Abstract
Acute lesions of the posterior medial orbitofrontal cortex (OFC) in humans may induce a state of reality confusion marked by confabulation, disorientation, and currently inappropriate actions. This clinical state is strongly associated with an inability to abandon previously valid anticipations, that is, extinction capacity. In healthy subjects, the filtering of memories according to their relation with ongoing reality is associated with activity in posterior medial OFC (area 13) and electrophysiologically expressed at 220–300 ms. These observations indicate that the human OFC also functions as a generic reality monitoring system. For this function, it is presumably more important for the OFC to evaluate the current behavioral appropriateness of anticipations rather than their hedonic value. In the present study, we put this hypothesis to the test. Participants performed a reversal learning task with intermittent absence of reward delivery. High-density evoked potential analysis showed that the omission of expected reward induced a specific electrocortical response in trials signaling the necessity to abandon the hitherto reward predicting choice, but not when omission of reward had no such connotation. This processing difference occurred at 200–300 ms. Source estimation using inverse solution analysis indicated that it emanated from the posterior medial OFC. We suggest that the human brain uses this signal from the OFC to keep thought and behavior in phase with reality.
Highlights
Acute lesions of the posterior medial orbitofrontal cortex (OFC) or structures directly connected with it may induce a state of dramatic reality confusion in human subjects: The patients confabulate recent experiences that never took place, are disoriented, confusing the time, place, and their current role, and enact ideas that do not apply to current reality [1,2]
The present study indicates that the behavioral relevance of an outcome may be a stronger driver of early human cerebral activity than hedonic value
Extinction trials evoked distinct electrocortical responses already at an early stage of processing between 200–300 ms, which were evident in the waveform analysis (Figure 2) and induced a significantly different overall electrocortical map configuration (Figure 3)
Summary
Acute lesions of the posterior medial orbitofrontal cortex (OFC) or structures directly connected with it may induce a state of dramatic reality confusion in human subjects: The patients confabulate recent experiences that never took place, are disoriented, confusing the time, place, and their current role, and enact ideas (e.g., going to work) that do not apply to current reality [1,2]. The primate posterior medial OFC –the area damaged or disconnected in the patients– has a high density of neurons that fire when anticipated outcomes (rewards) fail to occur [20,22] In analogy to these observations in animals, we hypothesized that the reality confusion of our patients reflected absence of, or the inability to make use of, the orbitofrontal signal which would normally indicate the nonoccurrence of anticipated outcomes, that is, the neural signal that normally underlies extinction [2]. Apart from traditional waveform analysis, we used advanced ERP topographic mapping techniques to estimate the generators of the electrocortical activity
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