The medial temporal lobe (MTL) is critical for mnemonic functions, navigation and social cognition. For many of these higher-order cognitive processes, correlates of single-neuron responses have been found in different regions of human MTL. Amygdala neurons respond to emotional stimuli [1], while hippocampus (HC) and entorhinal cortex (EC) neurons encode memory [2] and navigation [3]. Efficient encoding of task covariates depends on neurons with mixed selectivity, found in rodent subiculum and EC [4]. While this coding scheme has been described in human MTL [5], it remains elusive whether it is applied differentially in different contexts.
Methods We investigated the activity of 500 neurons in human MTL while participants watched a movie with alternating neutral and emotionally charged clips [6]. To model neuronal firing rates, we applied a Generalized Linear Model, using three covariates: trial type (Face/Landscape), size of the dominant object, and its movement across frames. We then implemented a model selection procedure to identify neurons specifically tuned to each covariate. Results We found the highest number of neurons encoding the difference between trials of landscapes versus emotional faces (14%). A smaller but substantial population of neurons showed specificity for the main object size and degree of movement (5% and 6%). Additionally, 3% of neurons demonstrated mixed selectivity, responding to the combination of at least two visual features. Despite the amygdala's established role in processing of emotional stimuli, we found only a slightly increased number of neurons specific to emotional trials in the amygdala compared to HC and EC, and the difference in the proportion of emotionally responsive neurons across the MTL was not statistically significant (P > 0.9, χ² test). Discussion Overall, it suggests emotional stimulus processing is distributed across MTL regions and neurons encoding emotional stimuli may additionally show selectivity for other task features. The presence of mixed selectivity further highlights the integrative role of MTL neurons in processing complex visual and emotional information, potentially supporting flexible cognitive functions.
Acknowledgements We sincerely appreciate the time and contribution of all patients who participated in this study. We are also grateful to our colleagues and collaborators for their insightful discussions and support. We extend our deep gratitude to the clinical staff for their invaluable assistance in data collection. References 1.https://doi.org/10.1073/pnas.1323342111 2.https://doi.org/10.1523/jneurosci.1648-20.2020 3.https://doi.org/10.1038/nn.3466 4.https://doi.org/10.1016/j.celrep.2021.109175 5.https://doi.org/10.1016/j.celrep.2024.114071 6.https://doi.org/10.1038/s41597-020-00790-x
