A comparative analysis of the physiological properties of neurons in the anterolateral bed nucleus of the stria terminalis in the Mus musculus, Rattus norvegicus, and Macaca mulatta

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There is a growing literature that describes the importance of the anterior bed nucleus of the stria terminalis (BNST) in a variety of behaviors including anxiety behavior and drug addiction (Duvarci, Bauer, & Pare, 2009; Kalin, Shelton, Fox, Oakes, & Davidson, 2005; Mantsch et al., 2014; Pleil, Rinker, et al., 2015; Sullivan et al., 2004). Although most of this research has been done in rodents, there is also evidence from both human and nonhuman primate studies that supports the role of the BNST as a modulator of anxiety behavior, drug self‐administration, binge alcohol drinking, threat monitoring, and anticipatory anxiety (Alvarez, Chen, Bodurka, Kaplan, & Grillon, 2011; Fox et al., 2010; Macey, Smith, Nader, & Porrino, 2003; Pleil, Lowery‐Gionta, et al., 2015; Somerville, Whalen, & Kelley, 2010; Straube, Mentzel, & Miltner, 2007). These studies strongly indicate that the role of the BNST is conserved across species from the rodent to the primate, suggesting the structure of the BNST may be conserved as well.
The BNST is not a homogenous structure; the rat BNST can be divided into at least 16 unique subregions and contains numerous distinct cell populations (Bota, Sporns, & Swanson, 2012; Dong, Petrovich, Petrovich, Watts, et al., 2001; Dong & Swanson, 2004; Ju, Swanson, & Simerly, 1989; Larriva‐Sahd, 2006). The heterogeneity of the neurons in the BNST has been studied in depth in the anterolateral group of the BNST (BNSTALG) of the rat. Most neurons in BNSTALG of the rat can be classified into three distinct cell types based on their spiking and rectification properties and rebound depolarization in response to hyperpolarizing and depolarizing current injection: Type I (regular spiking [RS]), Type II (low‐threshold bursting [LTB]), and Type III (fast inward rectifiers; Hammack, Mania, & Rainnie, 2007; Rodriguez‐Sierra, Rodríguez‐Sierra, Turesson, & Pare, 2013). Importantly, these cell types differ in their expression profile of messenger RNA (mRNA) for ion channel subunits, serotonin receptor subtypes, and the neuropeptide, corticotropin releasing factor (CRF) (Dabrowska, Hazra, Guo, Li, et al., 2013; Guo, Hammack, Hazra, Levita, & Rainnie, 2009; Hazra et al., 2011). Hence, the electrophysiological cell type of neurons in the BNSTALG may be indicative of the functional role the neurons play in the circuit. Indeed, the vast majority of Type III neurons in the rat BNSTALG express the mRNA for CRF and are affected by stress in different ways than Type I and Type II cells (Dabrowska, Hazra, Guo, Li, et al., 2013), providing further evidence that cell types play different roles in the circuit.
Although Type I, Type II, and Type III cells were defined in the BNSTALG of the rat, the classification system has been appropriated for describing neurons in the mouse BNST (Silberman, Matthews, & Winder, 2013). Because the role of the BNST in anxiety behavior is conserved across multiple species, it is assumed that the neurons in the mouse BNST are similar to that of the rat. However, no study has systematically examined the neurons of the mouse BNSTALG to determine if the classification system defined in the rat is appropriate for describing neuron‐heterogeneity in the mouse. Similarly, it is unknown if the electrophysiological cell types of the rat BNSTALG are conserved in the BNST of the primate.
Here, we used whole‐cell patch clamp electrophysiology to describe the electrophysiological properties of BNSTALG neurons in the mouse, rat, and rhesus macaque using the classification system initially described in the rat (Hammack et al., 2007). We, then, compared and contrasted the physiological properties of neurons of the same cell type in the three species.
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