A Stable Sparse Fear Memory Trace in Human Amygdala

Pavlovian fear conditioning is highly conserved across species, providing a powerful model of aversive learning. In rodents, fear memory is stored and reactivated under the influence of the amygdala. There is no evidence for an equivalent mechanism in primates, and an opposite mechanism is proposed whereby primate amygdala contributes only to an initial phase of aversive learning, subsequently ceding fear memory to extra-amygdalar regions. Here, we reexamine this question by exploiting human high-resolution functional magnetic resonance imaging in conjunction with multivariate methods. By assuming a sparse neural coding, we show it is possible, at an individual subject level, to discriminate responses to conditioned (CS+ and CS-) stimuli in both basolateral and centro-cortical amygdala nuclei. The strength of this discrimination increased over time and was tightly coupled to the behavioral expression of fear, consistent with an expression of a stable fear memory trace. These data highlight that the human basolateral and centro-cortical amygdala support initial learning as well more enduring fear memory storage. A sparse neuronal representation for fear, here revealed by multivariate pattern classification, resolves why an enduring memory trace has proven elusive in previous human studies.