Bursting as a source of non-linear determinism in the firing patterns of nigral dopamine neurons

Jaeseung Jeong, Department of Psychiatry, Columbia College of Physicians and Surgeons, New York, NY, USA. jsjeong@kaist.ac.kr
Wei-Xing Shi, Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
Ralph Hoffman, Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
Jihoon Oh, College of Medicine, The Catholic University of Korea, Seoul, South Korea
John C. Gore, Vanderbilt University Institute of Imaging Science, Vanderbilt University, Nashville, TN, USA
Benjamin S. Bunney, Department of Psychiatry and Pharmacology, Yale University School of Medicine, New Haven, CT, USA
Bradley S. Peterson, Department of Psychiatry, Columbia College of Physicians and Surgeons and the New York State Psychiatric Institute, New York,NY, USA

Abstract

Nigral dopamine (DA) neurons in vivo exhibit complex firing patterns consisting of tonic single-spikes and phasic bursts that encode information for certain types of reward-related learning and behavior. Non-linear dynamical analysis has previously demonstrated the presence of a non-linear deterministic structure in complex firing patterns of DA neurons, yet the origin of this non-linear determinism remains unknown. In this study, we hypothesized that bursting activity is the primary source of non-linear determinism in the firing patterns of DA neurons. To test this hypothesis, we investigated the dimension complexity of inter-spike interval data recorded in vivo from bursting and non-bursting DA neurons in the chloral hydrate-anesthetized rat substantia nigra. We found that bursting DA neurons exhibited non-linear determinism in their firing patterns, whereas non-bursting DA neurons showed truly stochastic firing patterns. Determinism was also detected in the isolated burst and inter-burst interval data extracted from firing patterns of bursting neurons. Moreover, less bursting DA neurons in halothane-anesthetized rats exhibited higher dimensional spiking dynamics than do more bursting DA neurons in chloral hydrate-anesthetized rats. These results strongly indicate that bursting activity is the main source of low-dimensional, non-linear determinism in the firing patterns of DA neurons. This finding furthermore suggests that bursts are the likely carriers of meaningful information in the firing activities of DA neurons.