Single-Trial Learning of Novel Stimuli by Individual Neurons of the Human Hippocampus-Amygdala Complex

Abstract

The ability to distinguish novel from familiar stimuli allows nervous systems to rapidly encode significant events following even a single exposure to a stimulus. This detection of novelty is necessary for many types of learning. Neurons in the medial temporal lobe (MTL) are critically involved in the acquisition of long-term declarative memories. During a learning task, we recorded from individual MTL neurons in vivo using microwire electrodes implanted in human epilepsy surgery patients. We report here the discovery of two classes of neurons in the hippocampus and amygdala that exhibit single-trial learning: novelty and familiarity detectors, which show a selective increase in firing for new and old stimuli, respectively. The neurons retain memory for the stimulus for 24 hr. Thus, neurons in the MTL contain information sufficient for reliable novelty-familiarity discrimination and also show rapid plasticity as a result of single-trial learning.

The Neurobiological Foundations of Valuation in Human Decision Making Under Uncertainty

“…When contrasting choices involving ambiguity against those involving only pure risk, however, amygdala activation is strong. This is consistent with the amygdala's role in learning, for example, in in oddball and novelty tasks (Rutishauser, Mamelak et al 2006), and suggests that the amygdala signals a need for learning of the unknown probabilities. Further research is needed to discover the true role of amygdala under ambiguity.…”

Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas

“…Hippocampal neurons in monkeys (Brown and Xiang, 1998), rats (e.g., Otto and Eichenbaum, 1992), and humans (Davachi and Wagner, 2002;Rutishauser et al, 2006) do not show stimulus-selective activations or repetition-related firing patterns during delayed matching and nonmatching tasks that test item recognition. Instead, hippocampal neurons show only general responses to novelty or familiarity across a broad range of stimuli, suggesting a role in encoding the outcome of recognition experiences.…”

Intracranial neuronal ensemble recordings and analysis in epilepsy

“…Due to the frequent seizure involvement of the temporal lobe, numerous studies have been performed to understand emotional and memory processes. Human hippocampal neurons respond in a highly specific manner to complex stimulus features and categories (Fried et al, 1997), and are selective for the novelty of the stimulus (Rutishauser et al, 2006). In a free recall task, individual neurons are able to reactivate the pattern shown in the preceding learning period (Gelbard-Sagiv et al, 2008).…”