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Neumaier, J. F.

Publications and source records attributed to Neumaier, J. F..

9 recordsLinked to original sources

An oral fentanyl self-administration model reveals dissociable escalation and relapse phenotypes in outbred vs inbred mice

Fentanyl-related overdose deaths now commonly involve non-injection routes, yet preclinical opioid self-administration is modeled predominantly intravenously. Here we establish an oral fentanyl self-administration procedure in male and female inbred C57BL/6 and outbred CD1 mice that measures volitional intake, cue-driven seeking, extinction, and relapse. Mice self-administered oral fentanyl (70 {micro}g/mL) on a fixed-ratio 1 schedule across fifteen 3-hour sessions, followed by ten extinction sessions and a cued reinstatement test. A separate cohort underwent between-session dose thresholding across a quarter-log series from 222 to 22 {micro}g/mL. Seventy-five percent of mice acquired self-administration, with similar rates across genetic background and sex. Responding increased as fentanyl concentration fell, indicating dose-sensitivity toward a preferred drug level. C57BL/6 mice escalated intake and lever pressing across sessions, responded persistently early in extinction before declining, and reinstated pressing to a conditioned cue. CD1 mice consumed high levels from the outset with limited escalation and showed neither extinction nor cued reinstatement of pressing, but shortened their reward-port approach latency when cues returned. This shows that lever presses alone would have misclassified them as weakly conditioned. A composite severity score summing seven components of fentanyl-use risk varied continuously rather than splitting into high and low groups, even among inbred mice. Sex differences were largely confined to C57BL/6 mice, in which females showed stronger cue association and higher severity scores than males. These results reveal separable escalation-prone and relapse-prone phenotypes that track genetic background. Protocols, hardware specifications, and analysis code are openly available, lowering the barrier to adopting oral fentanyl self-administration.

neuroscience↗

Stars2Cells: Astrometric Tracking of Neurons Across Imaging Sessions

Chronic calcium imaging offers a window into how single neurons and ensemble activity change across days where identifying the same neurons from one session to the next is the prerequisite for answering questions regarding learning, drift, and plasticity over time. Yet only [~]2-3% of imaging laboratories publish longitudinal cross-session work, because existing registration tools depend on spatial-footprint or temporal correlations that degrade under repeated recording sessions. Here, we introduce Stars2Cells (S2C), a tracking pipeline inspired by astrometric plate-solving that represents each neurons local geometry as a four-dimensional quad descriptor invariant to rotation, translation, and uniform scaling. S2C operates purely on centroid coordinates and combines descriptor-space matching, Random Sample Consensus (RANSAC) verification, and Hungarian assignment. Across a synthetic benchmark of 1,262 paired runs spanning 100-1,000 neurons and 8 perturbation conditions plus 1 identity sanity-floor, S2C reached pooled F1 = 98.4% compared to the standard ROI-based matching of 36.0%. To show what this enables, we applied the pipeline to dorsomedial striatum (DMS) imaging during oral fentanyl behavioral-economics self-administration. Here, we show that a conserved population-rewarded lever press response in DMS masks near-complete single-neuron turnover. This representational-drift signature we demonstrated is invisible to the bulk photometry, and resolving it requires the same-cell tracking S2C provides. S2C is distributed as a GUI-driven standalone application for both macOS and Windows, requiring no Python, command line, or virtual environment setup.

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Miniscope Processing Suite (MPS): An Intuitive, No-Code, Scalable Pipeline for Long Duration Calcium Imaging

Miniscope calcium imaging provides a unique window into the activity of neurons during behavior while enabling spatial localization of individual cells across time. Despite its potential to revolutionize in vivo imaging alongside the rise of optogenetic tools, miniscopes remain underutilized. This gap may stem from the lack of an easy-to-use preprocessing software tailored to miniscope data. To address this need, we developed the first no-code end-to-end scalable pipeline for preprocessing large miniscope recordings: the Miniscope Processing Suite (MPS). MPS is the first implementation of Constrained Non-negative Matrix Factorization (CNMF) with Nonnegative Double Singular Value Decomposition (NNDSVD) initialization, multi-lasso segmentation, and parallelized temporal and spatial updates, enabling analysis of recordings exceeding three hours on a standard hardware. We tested a large dataset consisting of 28 operant behavior sessions (77 hrs, 7.26 TB of video data) on a single workstation. MPS completed the analysis in 55.6 hrs, (averaging 0.72 minute of processing time per minute of recording), which is 10-20X faster than traditional pipelines. Packaged as an easy downloadable plug-and-play software with a graphical user interface and requiring no coding or Git experience, MPS lowers the barrier to miniscope analysis while improving on current methodologies.

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Repeated fentanyl abstinence intensifies opioid withdrawal and induces a proinflammatory state in striatal microglia

Opioid withdrawal is a serious obstacle to self-initiated abstinence, and previous experiences of opioid withdrawal may exacerbate the severity of subsequent incidences. To study the impact of repeated opioid withdrawal episodes, we compared male and female mice after one or five cycles of fentanyl exposure and withdrawal. We selectively expressed hemagglutinin-tagged ribosomes (RiboTag) in microglia of transgenic mice to immunoprecipitate and sequence RNA actively undergoing translation (the "translatome") from striatal microglia during fentanyl withdrawal. Key changes were confirmed by RTqPCR of RiboTag RNA. Repeated bouts of fentanyl treatment and withdrawal impacted striatal microglia much more than a single cycle of fentanyl followed by withdrawal. Multiple withdrawal cycles reduced ramification of microglial processes, suggesting a more reactive cell state, and induced more severe behavioral withdrawal signs in mice. Five cycles of fentanyl exposure and withdrawal increased the expression of gene networks associated with innate immunity signaling. Indeed, 100% of the genes associated with the "microglia core sensome", were upregulated after five cycles of withdrawal. Together these results suggest that mouse striatal microglia initiate a proinflammatory response following five, but not one, opioid exposure and withdrawal experiences and suggest that drug therapies targeting microglial innate immune responses may mitigate the severe withdrawal associated with repeated opioid tolerance and withdrawal. Significance statementRepeated cycles of fentanyl administration and withdrawal caused worsened behavioral signs of withdrawal in mice. This is the first such study to directly examine the effects of repeated opioid withdrawal on mouse behavior. We also found that repeated opioid withdrawal increased the expression of RNAs related to the proinflammatory "microglia core sensome". Furthermore, microglia in the mouse striatum were present at a higher density with reduced ramification, which suggests that multiple opioid withdrawal experiences cause a significant change to microglial signaling-state.

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Rapid appearance of negative emotion during oral fentanyl self-administration in male and female rats

Opioid use disorder has become an epidemic in the United States, fueled by the widespread availability of fentanyl, which produces rapid and intense euphoria followed by severe withdrawal and emotional distress. We developed a new preclinical model of fentanyl seeking in outbred male and female rats using volitional oral self-administration that can be readily applied in labs without intravascular access. Using a traditional two lever operant procedure, rats learned to take oral fentanyl vigorously, escalated intake across sessions, and readily reinstated responding to conditioned cues after extinction. Oral self-administration also revealed individual and sex differences that are essential to studying substance use risk propensity. During a behavioral economics task, rats displayed inelastic demand curves and maintained stable intake across a wide range of fentanyl concentrations. Oral SA was also neatly patterned, with distinct " loading" and " maintenance" phases of responding within each session. Using our software DeepSqueak, we analyzed thousands of ultrasonic vocalizations (USVs), which are innate expressions of current emotional state in rats. Rats produced 50 kHz USVs during loading then shifted quickly to 22 kHz calls despite ongoing maintenance oral fentanyl taking, reflecting a transition to negative reinforcement. Using fiber photometry, we found that the lateral habenula differentially processed drug-cues and drug-consumption depending on affective state, with potentiated modulation by drug cues and consumption during the negative affective maintenance phase. Together, these results indicate a rapid progression from positive to negative reinforcement occurs even within an active drug taking session, revealing a within-session opponent process. Significance StatementThe United States opioid epidemic is defined by rampant and treatment resistant fentanyl use. Better understanding of neural substrates underlying this phenomenon is essential to slowing the opioid crisis. Intravenous and vapor self-administration (SA) are the standard models for studying fentanyl use in rodents, however they many carry pragmatic downsides. Here, we used a novel oral fentanyl self-administration model that provides key translational and technical benefits and can be readily applied in other labs to study the neurobiology of fentanyl SA. This method captured individual and sex differences necessary for studying substance use risk propensity and uncovered a rapid shift in affective state in rats, suggesting and shift from positive to negative reinforcement within each fentanyl taking session.

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Stress decreases serotonin tone in the nucleus accumbens to promote aversion and potentiate cocaine preference via decreased stimulation of 5-HT1B receptors

Stress-induced release of dynorphins (Dyn) activates kappa opioid receptors (KOR) in monoaminergic neurons to produce dysphoria and potentiate drug reward; however, the circuit mechanisms responsible for this effect are not known. We found that conditional deletion of KOR from Slc6a4 (SERT)-expressing neurons blocked stress-induced potentiation of cocaine conditioned place preference (CPP). Within the dorsal raphe nucleus (DRN), two overlapping populations of KOR-expressing neurons: Slc17a8 (VGluT3) and SERT, were distinguished functionally and anatomically. Optogenetic inhibition of these SERT+ neurons potentiated subsequent cocaine CPP, whereas optical inhibition of the VGluT3+ neurons blocked subsequent cocaine CPP. SERT+/VGluT3- expressing neurons were concentrated in the lateral aspect of the DRN. SERT projections from the DRN were observed in the medial nucleus accumbens (mNAc), but VGluT3 projections were not. Optical inhibition of SERT+ neurons produced place aversion, whereas optical stimulation of SERT+ terminals in the mNAc attenuated stress-induced increases in forced swim immobility and subsequent cocaine CPP. KOR neurons projecting to mNAc were confined to the lateral aspect of the DRN, and the principal source of dynorphinergic (Pdyn) afferents in the mNAc was from local neurons. Excision of Pdyn from the mNAc blocked stress-potentiation of cocaine CPP. Prior studies suggested that stress-induced dynorphin release within the mNAc activates KOR to potentiate cocaine preference by a reduction in 5-HT tone. Consistent with this hypothesis, a transient pharmacological blockade of mNAc 5-HT1B receptors potentiated subsequent cocaine CPP. 5-HT1B is known to be expressed on 5-HT terminals in NAc, and 5-HT1B transcript was also detected in Pdyn+, Adora2a+ and ChAT+ (markers for direct pathway, indirect pathway, and cholinergic interneurons, respectively). Following stress exposure, 5-HT1B transcript was selectively elevated in Pdyn+ cells of the mNAc. These findings suggest that Dyn/KOR regulates serotonin activation of 5HT1B receptors within the mNAc and dynamically controls stress response, affect, and drug reward.

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RiboTag-Seq Reveals the Activation of the Unfolded Protein Response in Striatal Microglia Induced by Ethanol Withdrawal

Repeated cycles of alcohol intoxication and withdrawal induce profound changes in gene expression that can contribute to the physiological and behavioral consequences of ethanol. Since neuroinflammation is an important consequence of these changes, we used a novel strategy to investigate the impact of repeated cycles of chronic intermittent ethanol vapor and withdrawal on the RNAs actively undergoing translation in microglia in striatum, a key region involved in the relapse to ethanol consumption. We performed deep sequencing of the "translatome" from striatal microglia of male and female RiboTag mice, yielding a snapshot of RNA translation during alcohol intoxication and after 8 hours of withdrawal. Chronic intermittent ethanol produced robust changes in the translatome, with increases in genes and pathways associated with cytokine signaling, indicating increased neuroinflammation and microglial activation. After 8 hours of ethanol withdrawal, many inflammatory pathways remained upregulated and phagocytotic and proapoptotic pathways were increased. Using unbiased network analysis, we identified gene modules that were differentially expressed in ethanol intoxicated vs. withdrawing animals. Genes associated with the unfolded protein response (UPR) were over-represented in one such module after withdrawal, including the transcription factor Ddit3 (CHOP), an important mediator of the UPR. We tested the impact of conditional knockout of CHOP from microglia specifically; following withdrawal from chronic intermittent ethanol, these mice had reduced thermoregulatory disturbances, anxiety-like behavior, and voluntary ethanol consumption compared to wild-type littermates. We conclude that CHOP and the UPR in microglia may be important targets for reducing the impact of withdrawal from chronic ethanol exposure.

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Stress induces divergent gene expression among lateral habenula efferent pathways

The lateral habenula (LHb) integrates critical information regarding aversive stimuli that shapes decision making and behavioral responses. The three major LHb outputs innervate dorsal raphe nucleus (DRN), ventral tegmental area (VTA), and the rostromedial tegmental nucleus (RMTg). LHb neurons that project to these targets are segregated and nonoverlapping, and this led us to consider whether they have distinct molecular phenotypes and adaptations to stress exposure. In order to capture a time-locked profile of gene expression after repeated forced swim stress, we used intersectional expression of RiboTag in rat LHb neurons and next-gen RNA sequencing to interrogate the RNAs actively undergoing translation from each of these pathways. The "translatome" in the neurons comprising these pathways was similar at baseline, but diverged after stress, especially in the neurons projecting to the RMTg. Using weighted gene co-expression network analysis, we found one module comprising genes downregulated after stress in the RMTg-projecting LHb neurons; there was an overrepresentation of genes associated with phosphoinositide 3 kinase (PI3K) signaling in this module. Reduced PI3K signaling in RMTg-projecting LHb neurons may be a compensatory adaptation that alters the functional balance of LHb outputs to GABAergic vs. monoaminergic neurons following repeated stress exposure.

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RiboTag-Seq Reveals a Compensatory cAMP Responsive Gene Network in Striatal Microglia induced by Morphine Withdrawal

Microglia have recently been implicated in dependence to opioids. To investigate this directly, we used RNA sequencing of ribosome associated RNAs from striatal microglia (RiboTag-Seq) after the induction of morphine tolerance and then the precipitation of withdrawal by naloxone. We detected large, inverse changes in RNA translation following opioid tolerance and withdrawal, and bioinformatics analysis revealed an intriguing upregulation of cAMP-associated genes that are involved in microglial motility, morphology, and interactions with neurons. Three-dimensional histological reconstruction of microglia revealed changes in process branching and termination following opioid tolerance that were rapidly reversed during withdrawal and were consistent with cAMP effects on microglia morphology. Direct activation of Gi-coupled DREADD receptors in microglia, rather than mimicking the effects of morphine, exacerbated opioid withdrawal. Together these indicate that microglial response to cAMP signaling can mitigate the rapid manifestations of opioid withdrawal.

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