Nucleus accumbens core medium spiny neuron electrophysiological properties and partner preference behavior in the adult male prairie vole, Microtus ochrogaster

Abstract

Medium spiny neurons (MSNs) in the nucleus accumbens have long been implicated in the neurobiological mechanisms that underlie numerous social and motivated behaviors as studied in rodents such as rats. Recently, the prairie vole has emerged as an important model animal for studying social behaviors, particularly regarding monogamy because of its ability to form pair bonds. However, to our knowledge, no study has assessed intrinsic vole MSN electrophysiological properties or tested how these properties vary with the strength of the pair bond between partnered voles. Here we performed whole cell patch-clamp recordings of MSNs in acute brain slices of the nucleus accumbens core (NAc) of adult male voles exhibiting strong and weak preferences for their respective partnered females. We first document vole MSN electrophysiological properties and provide comparison to rat MSNs. Vole MSNs demonstrated many canonical electrophysiological attributes shared across species but exhibited notable differences in excitability compared with rat MSNs. Second, we assessed male vole partner preference behavior and tested whether MSN electrophysiological properties varied with partner preference strength. Male vole partner preference showed extensive variability. We found that decreases in miniature excitatory postsynaptic current amplitude and the slope of the evoked action potential firing rate to depolarizing current injection weakly associated with increased preference for the partnered female. This suggests that excitatory synaptic strength and neuronal excitability may be decreased in MSNs in males exhibiting stronger preference for a partnered female. Overall, these data provide extensive documentation of MSN electrophysiological characteristics and their relationship to social behavior in the prairie vole. NEW & NOTEWORTHY This research represents the first assessment of prairie vole nucleus accumbens core medium spiny neuron intrinsic electrophysiological properties and probes the relationship between cellular excitability and social behavior.

Differential mitochondrial morphology in ventral striatal projection neuron subtypes

“…D2-MSNs of NAc core, as well as dorsal striatum, also display enhanced intrinsic excitability (Ade et al, 2008;Cepeda et al, 2008;Chan et al, 2012;Chuhma et al, 2011;Gertler et al, 2008;Kreitzer & Malenka, 2007;Ma et al, 2013;Pascoli et al, 2014;Willett et al, 2018). Thus, the smaller mitochondria observed in D2 MSNs may represent reduced fusion as addressed above.…”

“…D2-MSNs display increased sEPSC frequency in NAc core and shell (Ma et al, 2013); however, another study examining NAc MSN subtypes in prepubertal mice demonstrated reduced mEPSC frequency in D2-MSNs in NAc core (Willett et al, 2018). D2-MSNs display increased sEPSC frequency in NAc core and shell (Ma et al, 2013); however, another study examining NAc MSN subtypes in prepubertal mice demonstrated reduced mEPSC frequency in D2-MSNs in NAc core (Willett et al, 2018).…”

“…The projecting MSN subtypes in the dorsal striatum and NAc display distinct electrophysiological properties, which could be related to their differences in dendritic mitochondrial morphology. D2-MSNs display increased sEPSC frequency in NAc core and shell (Ma et al, 2013); however, another study examining NAc MSN subtypes in prepubertal mice demonstrated reduced mEPSC frequency in D2-MSNs in NAc core (Willett et al, 2018). Increased smaller size mitochondria is associated with enhanced fission, which mediates structural and synaptic plasticity (Cassidy-Stone et al, 2008;Chen et al, 2007;Divakaruni et al, 2018;Ishihara et al, 2009;Li et al, 2004).…”

“…Further, studies have demonstrated distinct electrophysiological properties in MSN subtypes that correspond to morphological properties (Ade, Janssen, Ortinski, & Vicini, 2008;Cepeda et al, 2008;Chan et al, 2012;Chuhma, Tanaka, Hen, & Rayport, 2011;Gertler, Chan, & Surmeier, 2008;Kreitzer & Malenka, 2007;Ma et al, 2013;Pascoli et al, 2014;Willett et al, 2018). Further, studies have demonstrated distinct electrophysiological properties in MSN subtypes that correspond to morphological properties (Ade, Janssen, Ortinski, & Vicini, 2008;Cepeda et al, 2008;Chan et al, 2012;Chuhma, Tanaka, Hen, & Rayport, 2011;Gertler, Chan, & Surmeier, 2008;Kreitzer & Malenka, 2007;Ma et al, 2013;Pascoli et al, 2014;Willett et al, 2018).…”

“…pallidal regions including globus pallidus external (dorsal striatum) and ventral pallidum (NAc), although NAc D2-MSNs also send projections to the lateral hypothalamus. Further, studies have demonstrated distinct electrophysiological properties in MSN subtypes that correspond to morphological properties (Ade, Janssen, Ortinski, & Vicini, 2008;Cepeda et al, 2008;Chan et al, 2012;Chuhma, Tanaka, Hen, & Rayport, 2011;Gertler, Chan, & Surmeier, 2008;Kreitzer & Malenka, 2007;Ma et al, 2013;Pascoli et al, 2014;Willett et al, 2018). These properties are altered in MSN subtypes in diseased states including neurodegeneration, addiction, stress-induced affective behavior, pain, and repetitive behaviors (Chen et al, 2017;Fieblinger et al, 2014;Francis et al, 2015Francis et al, , 2017Galvan, Andre, Wang, Cepeda, & Levine, 2012;Graziane et al, 2016;Hearing et al, 2016;Heinsbroek et al, 2017;Kim, Park, Lee, Park, & Kim, 2011;LeGates et al, 2018;Lim, Huang, Grueter, Rothwell, & Malenka, 2012;Massaly et al, 2019;Ren et al, 2016;Rothwell et al, 2014;Schwartz et al, 2014;Terrier, Luscher, & Pascoli, 2016).…”