Abstract
The firing activity of ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) dopaminergic (DA) neurons is an important factor in shaping DA release and its role in motivated behavior. Dendrites in DA neurons are the main postsynaptic compartment and, along with cell body and axon initial segment, contribute to action potential generation and firing pattern. In this study, the organization of the dendritic domain in individual VTA and SNc DA neurons of adult male mice, and their relationship to in vivo spontaneous firing, are described. In comparison with dorsal VTA DA neurons, ventrally located VTA neurons (as measured by cell body location) possess a shorter total dendritic length and simpler dendritic architecture, and exhibit the most irregular in vivo firing patterns among DA neurons. In contrast, for DA neurons in the SNc, the higher irregularity of firing was related to a smaller dendritic domain, as measured by convex hull volumes. However, firing properties were also related to the specific regional distribution of the dendritic tree. Thus, VTA DA neurons with a larger extension of their dendritic tree within the parabrachial pigmented (PBP) nucleus fired more regularly compared with those with relatively more dendrites extending outside the PBP. For DA neurons in the SNc, enhanced firing irregularity was associated with a smaller proportion of dendrites penetrating the substantia nigra pars reticulata. These results suggest that differences in dendritic morphology contribute to the in vivo firing properties of individual DA neurons, and that the existence of region-specific synaptic connectivity rules that shape firing diversity.
Highlights
Dopaminergic neurons of the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA) are involved in important brain functions, such as movement, behavioral reinforcement, and learning (Wise, 2004; Schultz, 2007; Fahn, 2008; Redgrave et al, 2008; Berke, 2018)
The animals were obtained from the animal house at the Faculty of Biological Sciences, Pontificia Universidad Católica de Chile, and were approved by the Ethics Committees of the School of Medicine of the Pontificia Universidad Católica de Chile which conform to the guidelines of the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) and the United States National Institutes of Health (NIH)
First: what are the architectural characteristics that define the dendritic domain of individual mouse SNc and VTA DA neurons? And, second: does the dendritic domain architecture relate to in vivo spontaneous firing activity at the individual cell level? To address these questions, we reconstructed the somatodendritic domain of DA neurons in 3D
Summary
Dopaminergic neurons of the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA) are involved in important brain functions, such as movement, behavioral reinforcement, and learning (Wise, 2004; Schultz, 2007; Fahn, 2008; Redgrave et al, 2008; Berke, 2018). Anatomical studies demonstrated that in SNc and VTA DA neurons the vast majority of synaptic inputs occurs in the dendritic field (Rinvik and Grofová, 1970; Bolam and Smith, 1990; Bayer and Pickel, 1991; Henny et al, 2012) as compared with less frequent innervation of somatic (Rinvik and Grofová, 1970) or axon initial segment (González-Cabrera et al, 2017) compartments This is in line with evidence from single cell reconstructions that show dendrites account for up to 90% of the somatodendritic surface in nigral neurons (Meza et al, 2018). Considering the role that synaptic inputs play in the firing behavior of DA neurons, understanding how the dendritic domain is organized in this population and how it relates to single cell behavior in vivo is a critical issue to examine
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