Salience processing by glutamatergic neurons in the ventral pallidum

Wang, Fang; Zhang, Juen; Yuan, Yuan; Chen, Ming; Gao, Zilong; Zhan, Shulu; Fan, Chengyu; Sun, Wenzhi; Hu, Ji

doi:10.1016/j.scib.2019.11.029

Cited by 13 publications

(17 citation statements)

References 51 publications

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“…VP neurons showing firing increases to a reward cue and decreases to an aversive cue have also been observed in monkeys 44 . Consistent across both studies, the VP contained a separate population that showed firing increases to both reward and aversive cues, indicative of salience signaling 19,[44][45][46] . Salience signaling has been most strongly linked to VP glutamate neurons 45 .…”

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confidence: 55%

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Ventral pallidum neurons dynamically signal relative threat

2021

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The ventral pallidum (VP) is anatomically poised to contribute to threat behavior. Recent studies report a VP population that scales firing increases to reward but decreases firing to aversive cues. Here, we tested whether firing decreases in VP neurons serve as a neural signal for relative threat. Single-unit activity was recorded while male rats discriminated cues predicting unique foot shock probabilities. Rats’ behavior and VP single-unit firing discriminated danger, uncertainty, and safety cues. Two populations of VP neurons dynamically signaled relative threat, decreasing firing according to foot shock probability during early cue presentation, but disproportionately decreasing firing to uncertain threat as foot shock drew near. One relative threat population increased firing to reward, consistent with a bi-directional signal for general value. The second population was unresponsive to reward, revealing a specific signal for relative threat. The results reinforce anatomy to reveal the VP as a neural source of a dynamic, relative threat signal.

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confidence: 55%

“…Consistent across both studies, the VP contained a separate population that showed firing increases to both reward and aversive cues, indicative of salience signaling 19 , 44 – 46 . Salience signaling has been most strongly linked to VP glutamate neurons 45 .…”

Section: Introductionmentioning

confidence: 99%

Ventral pallidum neurons dynamically signal relative threat

2021

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“…VP neurons showing firing increases to rewarding cues and decreases to aversive cues have also been observed in monkeys 40 . Consistent across both studies, mouse and monkey VP contained a separate population that showed firing increases to rewarding and aversive cues, indicative of salience signaling 18,[40][41][42] .…”

Section: Introductionsupporting

confidence: 55%

“…The VP is essential to reward behavior 15,23,28 and recent evidence reveals the VP as a neural source of relative reward value 35 . A host of studies implicate the VP in aversive learning and behavior [18][19][20]36,[39][40][41]55,63,67 .…”

Section: Cue-excited Neurons Increase Firing To Rewardmentioning

confidence: 99%

Ventral pallidum neurons signal relative threat

Moaddab

Ray

McDannald

2020

Preprint

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Ventral pallidum (VP) neurons scale firing increases to reward value and decrease firing to aversive cues.Anatomical connectivity suggests a critical role for the VP in threat-related behavior. Here we tested whether firing decreases in VP neurons conform to relative threat by recording single units while male rats discriminated cues predicting unique foot shock probabilities. Rats behavior and VP single unit firing discriminated danger, uncertainty and safety cues. We found that two VP populations (Low firing and Intermediate firing) signaled relative threat, proportionally decreased firing according shock probability: danger < uncertainty < safety. Low firing neurons showed reward firing increases, consistent with a general signal for relative value.Intermediate firing neurons were unresponsive to reward, revealing a specific signal for relative threat. The results suggest an integral role for the VP in threat-related behavior. ResultsMale, Long Evans rats (n = 14) were moderately food-deprived and trained to nose poke in a central port in order to receive a reward (food pellet). Nose poking was reinforced throughout fear discrimination, but poke-reward and cue-shock contingencies were independent. During fear discrimination, three distinct auditory cues predicted unique foot shock probabilities: danger (p=1.00), uncertainty (p=0.25), and safety (p=0.00) (Fig. 1a). Each fear discrimination session consisted of 16 trials: 4 danger, 2 uncertainty-shock, 6 uncertainty-omission, and 4 safety, mean 3.5 min inter-trial interval (ITI). Each trial started with a 20 s baseline period followed by 10 s cue presentation. Foot shock (0.5 mA, 0.5 s) was administered 2 s following cue offset on shock trials (Fig. 1b). Trial order was randomized for each rat, each session. Fear was measured by the suppression of rewarded nose poking. A suppression ratio was calculated by comparing nose poke rates during baseline and cue periods (see methods). After eight discrimination sessions, rats were implanted with drivable microelectrode bundles dorsal to the VP (Fig. 1c). Following recovery, single unit activity was recorded while rats underwent fear discrimination. The microelectrode bundle was advanced through

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“…For example, VP GABA neurons fire in response to water rewards and their predictors in mice, especially when those rewards are particularly valuable due to thirst (Stephenson-Jones et al, 2020). Optogenetic activation of mouse VP GABA neurons elicits food intake and operant water seeking (Zhu et al, 2017; Stephenson-Jones et al, 2020) and is reinforcing (Zhu et al, 2017; Faget et al, 2018), while optogenetic stimulation of VP glutamate neurons elicits aversive responses and promotes operant avoidance (Faget et al, 2018; Tooley et al, 2018; Levi et al, 2019; Stephenson-Jones et al, 2020)—though a recent report suggests that VP glutamate neurons may mediate salience irrespective of valence (Wang et al, 2020). None of these prior mouse studies indicated a role for VP GABA neurons in aversive motivation, but they did not examine more complex types of aversive responding.…”

Section: Discussionmentioning

confidence: 99%

Ventral Pallidum GABA Neurons Mediate Motivation Underlying Risky Choice

Farrell¹,

Esteban²,

Faget³

et al. 2020

Preprint

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Pursuing rewards while avoiding danger is an essential function of nervous systems. Here, we examine a new mechanism helping rats negotiate the balance between risk and reward when making high-stakes decisions. Specifically, we focus on GABA neurons within an emerging mesolimbic circuit nexus, the ventral pallidum (VP). These neurons play a distinct role from other VP neurons in simple motivated behaviors in mice, but their roles in more complex motivated behaviors is unknown. Here, we interrogate the behavioral functions of VP GABA neurons in male and female transgenic GAD1:Cre rats (and wildtype littermates), using reversible chemogenetic inhibition. Employing a behavioral assay of risky decision making, and of the food-seeking and shock-avoidance components of this task, we show that engaging inhibitory Gi/o signaling specifically in VP GABA neurons suppresses motivation to pursue highly salient palatable foods, and notably, also motivation to avoid being shocked. In contrast, inhibiting these neurons did not affect seeking of low-value food, or free consumption even of palatable food, nor did it impact unconditioned affective responses to shock. Accordingly, when rats considered whether to pursue food despite potential for shock in a risky decision-making task, inhibiting VP GABA neurons caused rats to more readily select a small but safe reward over a large but dangerous one--the first demonstration of a VP role in complex decision making. Together, results indicate that VP GABA neurons are critical for high-stakes adaptive responding that is necessary for life, but which might also malfunction in psychiatric disease.

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Salience processing by glutamatergic neurons in the ventral pallidum

Cited by 13 publications

References 51 publications

Ventral pallidum neurons dynamically signal relative threat

Ventral pallidum neurons dynamically signal relative threat

Ventral pallidum neurons signal relative threat

Ventral Pallidum GABA Neurons Mediate Motivation Underlying Risky Choice

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