Alcohol Consumption during Adolescence in a Mouse Model of Binge Drinking Alters the Intrinsic Excitability and Function of the Prefrontal Cortex through a Reduction in the Hyperpolarization-Activated Cation Current
Open accessAbstract
Periodic episodes of excessive alcohol consumption (“binge drinking”) occur frequently among adolescents, and early binge drinking is associated with an increased risk of alcohol use disorders later in life. The PFC undergoes significant development during adolescence and hence may be especially susceptible to the effects of binge drinking. In humans and in animal models, adolescent alcohol exposure is known to alter PFC neuronal activity and produce deficits in PFC-dependent behaviors, such as decision making, response inhibition, and working memory. Using a voluntary intermittent access to alcohol (IA EtOH) procedure in male mice, we demonstrate that binge-level alcohol consumption during adolescence leads to altered drinking patterns and working memory deficits in young adulthood, two outcomes that suggest medial PFC dysfunction. We recorded from pyramidal neurons (PNs) in the prelimbic subregion of the medial PFC in slices obtained from mice that had IA EtOH and found that they display altered excitability, including a hyperpolarization of the resting membrane potential and reductions in the hyperpolarization-activated cation current (Ih) and in intrinsic persistent activity (a mode of neuronal firing that is dependent on Ih). Many of these effects on intrinsic excitability were sustained following abstinence and observed in mice that showed working memory deficits. In addition, we found that resting membrane potential and the Ih-dependent voltage “sag” in prelimbic PFC PNs are developmentally regulated during adolescence, suggesting that adolescent alcohol exposure may compromise PFC function by arresting the normal developmental trajectory of PN intrinsic excitability. SIGNIFICANCE STATEMENT Binge alcohol drinking during adolescence has negative consequences for the function of the developing PFC. Using a mouse model of voluntary binge drinking during adolescence, we found that this behavior leads to working memory deficits and altered drinking behavior in adulthood. In addition, we found that adolescent drinking is associated with specific changes to the intrinsic excitability of pyramidal neurons in the PFC, reducing the ability of these neurons to generate intrinsic persistent activity, a phenomenon thought to be important for working memory. These findings may help explain why human adolescent binge drinkers show performance deficits on tasks mediated by the PFC.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Recent studies have reported deficits in recall of an extinguished fear response, deficits in reversal learning, and impaired working memory following adolescent alcohol exposure.
“Recent studies have reported deficits in recall of an extinguished fear response [54], deficits in reversal learning [43], and impaired working memory [55, 56] following AAE.”
From Consequences of adolescent drug use (2023) · cites this paper as [55]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Casey, B. J., Jones, R. M., & Hare, T. A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.010 · Cited by 3,345 · see citing works
Kessler, R. C. (1997) · Archives of General Psychiatry · doi:10.1001/archpsyc.1997.01830160031005 · Cited by 2,085 · see citing works
Grant, B. F., & Dawson, D. A. (1997) · Journal of Substance Abuse · doi:10.1016/s0899-3289(97)90009-2 · Cited by 1,793 · see citing works
Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.09.006 · Cited by 1,329 · see citing works
Synaptic reverberation underlying mnemonic persistent activity
Wang, X.-J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01868-3 · Cited by 1,059 · see citing works
The Neuropsychopharmacology of Fronto-Executive Function: Monoaminergic Modulation
Robbins, T. W., & Arnsten, A. F. T. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135535 · Cited by 957 · see citing works
Gamma and Beta Bursts Underlie Working Memory
Lundqvist, M., Rose, J., Herman, P., Brincat, S. L., Buschman, T. J., & Miller, E. K. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.028 · Cited by 846 · see citing works
Graded persistent activity in entorhinal cortex neurons
Egorov, A. V., Hamam, B. N., Fransén, E., Hasselmo, M. E., & Alonso, A. A. (2002) · Nature · doi:10.1038/nature01171 · Cited by 769 · see citing works
Beyond simple models of self-control to circuit-based accounts of adolescent behavior
Casey, B. J. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015156 · Cited by 742 · see citing works
Wang, M., Ramos, B. P., Paspalas, C. D., Shu, Y., Simen, A., Duque, A., Vijayraghavan, S., Brennan, A., Dudley, A., Nou, E., et al. (2007) · Cell · doi:10.1016/j.cell.2007.03.015 · Cited by 672 · see citing works
Thalamic projections sustain prefrontal activity during working memory maintenance
Bolkan, S. S., Stujenske, J. M., Parnaudeau, S., Spellman, T., Rauffenbart, C., Abbas, A. I., Harris, A. Z., Gordon, J. A., & Kellendonk, C. (2017) · Nature Neuroscience · doi:10.1038/nn.4568 · Cited by 521 · see citing works
Kellendonk, C., Simpson, E. H., Polan, H. J., Malleret, G., Vronskaya, S., Winiger, V., Moore, H., & Kandel, E. R. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.023 · Cited by 520 · see citing works
Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex
Gläscher, J., Adolphs, R., Damasio, H., Bechara, A., Rudrauf, D., Calamia, M., Paul, L. K., & Tranel, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206608109 · Cited by 476 · see citing works
Dynamics of Population Code for Working Memory in the Prefrontal Cortex
Baeg, E. H., Kim, Y. B., Huh, K., Mook-Jung, I., Kim, H. T., & Jung, M. W. (2003) · Neuron · doi:10.1016/s0896-6273(03)00597-x · Cited by 338 · see citing works
Binge Drinking, Cognitive Performance and Mood in a Population of Young Social Drinkers
Townshend, J. M., & Duka, T. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000156453.05028.f5 · Cited by 337 · see citing works
Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior
Crews, F. T., Vetreno, R. P., Broadwater, M., & Robinson, D. L. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.012138 · Cited by 332 · see citing works
Nolan, M. F., Malleret, G., Lee, K. H., Gibbs, E., Dudman, J. T., Santoro, B., Yin, D., Thompson, R. F., Siegelbaum, S. A., Kandel, E. R., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00884-5 · Cited by 320 · see citing works
Seizure-Induced Plasticity of h Channels in Entorhinal Cortical Layer III Pyramidal Neurons
Shah, M. M., Anderson, A. E., Leung, V. C. M., Lin, X., & Johnston, D. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.011 · Cited by 288 · see citing works
Projection-Specific Neuromodulation of Medial Prefrontal Cortex Neurons
Dembrow, N. C., Chitwood, R. A., & Johnston, D. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3644-10.2010 · Cited by 281 · see citing works
Narayanan, R., & Johnston, D. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.033 · Cited by 257 · see citing works
Role of Prefrontal Persistent Activity in Working Memory
Riley, M. R., & Constantinidis, C. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00181 · Cited by 251 · see citing works
Plasticity of intrinsic neuronal properties in CNS disorders
Beck, H., & Yaari, Y. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2371 · Cited by 238 · see citing works
Chronic Alcohol Exposure Alters Behavioral and Synaptic Plasticity of the Rodent Prefrontal Cortex
Kroener, S., Mulholland, P. J., New, N., Gass, J. T., Becker, H. C., & Chandler, L. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037541 · Cited by 236 · see citing works
Koss, W. A., Belden, C. E., Hristov, A. D., & Juraska, J. M. (2014) · Synapse · doi:10.1002/syn.21716 · Cited by 228 · see citing works
Gee, S., Ellwood, I., Patel, T., Luongo, F., Deisseroth, K., & Sohal, V. S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5835-11.2012 · Cited by 214 · see citing works
Optogenetic dissection of medial prefrontal cortex circuitry
Riga, D., Matos, M. R., Glas, A., Smit, A. B., Spijker, S., & Van den Oever, M. C. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00230 · Cited by 208 · see citing works
Pyramidal Neurons in Prefrontal Cortex Receive Subtype-Specific Forms of Excitation and Inhibition
Lee, A. T., Gee, S. M., Vogt, D., Patel, T., Rubenstein, J. L., & Sohal, V. S. (2014) · Neuron · doi:10.1016/j.neuron.2013.10.031 · Cited by 201 · see citing works
Gass, J. T., Glen, W. B., McGonigal, J. T., Trantham-Davidson, H., Lopez, M. F., Randall, P. K., Yaxley, R., Floresco, S. B., & Chandler, L. J. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.109 · Cited by 197 · see citing works
Alcohol and the prefrontal cortex
Abernathy, K., Chandler, L. J., & Woodward, J. J. (2010) · International Review of Neurobiology · doi:10.1016/s0074-7742(10)91009-x · Cited by 196 · see citing works
The effect of alcohol use on human adolescent brain structures and systems
Squeglia, L. M., Jacobus, J., & Tapert, S. F. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-62619-6.00028-8 · Cited by 190 · see citing works
Substance Abuse Among Adolescents
Sussman, S. Y., Skara, S. N., & Ames, S. L. (2008) · Substance Use & Misuse · doi:10.1080/10826080802297302 · Cited by 188 · see citing works
Altered Brain Developmental Trajectories in Adolescents After Initiating Drinking
Pfefferbaum, A., Kwon, D., Brumback, T., Thompson, W. K., Cummins, K. M., Tapert, S. F., Brown, S. A., Colrain, I. M., Baker, F. C., Prouty, D., et al. (2017) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2017.17040469 · Cited by 182 · see citing works
Cholinergic modulation of a specific memory function of prefrontal cortex
Croxson, P. L., Kyriazis, D. A., & Baxter, M. G. (2011) · Nature Neuroscience · doi:10.1038/nn.2971 · Cited by 166 · see citing works
Murray, A., Wołoszynowska-Fraser, M. U., Ansel-Bollepalli, L., Marshall-Phelps, K. L., Foggetti, A., Crouch, B., Riedel, G., & Wulff, P. (2015) · Scientific Reports · doi:10.1038/srep16778 · Cited by 165 · see citing works
Santoro, B., Piskorowski, R. A., Pian, P., Hu, L., Liu, H., & Siegelbaum, S. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.009 · Cited by 164 · see citing works
Cortical HCN channels: Function, trafficking and plasticity
Shah, M. M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2013.270058 · Cited by 160 · see citing works
Squeglia, L. M., Pulido, C., Wetherill, R. R., Jacobus, J., Brown, G. G., & Tapert, S. F. (2012) · Journal of Studies on Alcohol and Drugs · doi:10.15288/jsad.2012.73.749 · Cited by 154 · see citing works
Intrinsic plasticity: an emerging player in addiction
Kourrich, S., Calu, D. J., & Bonci, A. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn3877 · Cited by 151 · see citing works
Wilcox, M. V., Carlson, V. C. C., Sherazee, N., Sprow, G. M., Bock, R., Thiele, T. E., Lovinger, D. M., & Alvarez, V. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.230 · Cited by 140 · see citing works
Rau, A. R., Chappell, A. M., Butler, T. R., Ariwodola, O. J., & Weiner, J. L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0384-15.2015 · Cited by 136 · see citing works
Vulnerability for Alcohol Use Disorder and Rate of Alcohol Consumption
Gowin, J. L., Sloan, M. E., Stangl, B. L., Vatsalya, V., & Ramchandani, V. A. (2017) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2017.16101180 · Cited by 134 · see citing works
Trantham‐Davidson, H., Glover, E. J., Gass, J. T., Lopez, M. F., Mulholland, P. J., Centanni, S. W., Floresco, S., & Chandler, L. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0623-13.2014 · Cited by 128 · see citing works
Nixon, K., & McClain, J. A. (2010) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e32833864fe · Cited by 126 · see citing works
Ishikawa, A., Ambroggi, F., Nicola, S. M., & Fields, H. L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0253-08.2008 · Cited by 125 · see citing works
Alcohol Reduces Prefrontal Cortical Excitability in Humans: A Combined TMS and EEG Study
Kähkönen, S., Wilenius, J., Nikulin, V. V., Ollikainen, M., & Ilmoniemi, R. J. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300099 · Cited by 123 · see citing works
Meléndez, R. I. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01383.x · Cited by 121 · see citing works
Santello, M., & Nevian, T. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.003 · Cited by 118 · see citing works
Ethanol Inhibits Persistent Activity in Prefrontal Cortical Neurons
Tu, Y., Kroener, S., Abernathy, K., Lapish, C. C., Seamans, J. K., Chandler, L. J., & Woodward, J. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5378-06.2007 · Cited by 118 · see citing works
Crego, A., Holguı́n, S. R., Parada, M., Mota, N., Corral, M., & Cadaveira, F. (2010) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.11.020 · Cited by 105 · see citing works
Nimitvilai, S., Lopez, M. F., Mulholland, P. J., & Woodward, J. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.250 · Cited by 99 · see citing works
Vargas, W. M., Bengston, L., Gilpin, N. W., Whitcomb, B. W., & Richardson, H. N. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3189-13.2014 · Cited by 99 · cited 2× · see citing works
“Furthermore, our findings are in agreement with several rodent studies in which performance on PFC-dependent tasks was negatively influenced by chronic alcohol exposure (Gass et al., 2014; Vargas et al., 2014; McMurray et al., 2016; Schindler et al., 2016).”
BackgroundResultAnimal Models of Excessive Alcohol Consumption in Rodents
Becker, H. C. (2012) · Current topics in behavioral neurosciences · doi:10.1007/978-3-642-28720-6_203 · Cited by 96 · see citing works
Brewster, A. L., Chen, Y., Bender, R. A., Yeh, A., Shigemoto, R., & Baram, T. Z. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk021 · Cited by 96 · see citing works
Prelimbic and Infralimbic Neurons Signal Distinct Aspects of Appetitive Instrumental Behavior
Burgos-Robles, A., Bravo-Rivera, H., & Quirk, G. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057575 · Cited by 95 · see citing works
Thuault, S., Malleret, G., Constantinople, C. M., Nicholls, R. E., Chen, I., Zhu, J., Panteleyev, A. A., Vronskaya, S., Nolan, M. F., Bruno, R. M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2427-12.2013 · Cited by 91 · see citing works
Matos, S. C., Zhang, Z., & Séguéla, P. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0799-15.2015 · Cited by 85 · see citing works
Yoshimura, M., & Tabakoff, B. (1995) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1995.tb01004.x · Cited by 82 · see citing works
Salling, M. C., Faccidomo, S., Li, C., Psilos, K. E., Galunas, C., Spanos, M., Agoglia, A. E., Kash, T. L., & Hodge, C. W. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.10.020 · Cited by 79 · see citing works
Self-citationEthanol Selectively Attenuates NMDAR‐Mediated Synaptic Transmission in the Prefrontal Cortex
Weitlauf, C., & Woodward, J. J. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00625.x · Cited by 77 · see citing works
Badanich, K. A., Mulholland, P. J., Beckley, J. T., Trantham‐Davidson, H., & Woodward, J. J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.12 · Cited by 74 · see citing works
Ragozzino, M. E., & Kesner, R. P. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3823 · Cited by 69 · see citing works
Han, Y. S., Noam, Y., Lewis, A. S., Gallagher, J. J., Wadman, W. J., Baram, T. Z., & Chetkovich, D. M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.236125 · Cited by 63 · see citing works
Animal Models of Excessive Alcohol Consumption in Rodents
Becker, H. C. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_203 · Cited by 57 · see citing works
An integrated brain–behavior model for working memory
Moser, D. A., Doucet, G. E., Ing, A., Dima, D., Schumann, G., Bilder, R. M., & Frangou, S. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.247 · Cited by 54 · see citing works
Han, Y. S., Heuermann, R. J., Lyman, K. A., Fisher, D. W., Ismail, Q.-A., & Chetkovich, D. M. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.99 · Cited by 53 · see citing works
Schindler, A. G., Soden, M. E., Zweifel, L. S., & Clark, J. J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4394-15.2016 · Cited by 52 · see citing works
Salling, M. C., & Harrison, N. L. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00714.2013 · Cited by 50 · see citing works
Self-citationMüller‐Oehring, E. M., Kwon, D., Nagel, B. J., Sullivan, E. V., Chu, W., Torsten Rohlfing, B., Prouty, D., Nichols, B. N., Poline, J., Tapert, S. F., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx014 · Cited by 50 · see citing works
Hwa, L. S., Nathanson, A. J., Shimamoto, A., Tayeh, J. K., Wilens, A. R., Holly, E. N., Newman, E. L., DeBold, J. F., & Miczek, K. A. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3925-y · Cited by 47 · see citing works
Bender, R. A., Galindo, R., Mameli, M., Gonzalez‐Vega, R., Valenzuela, C. F., & Baram, T. Z. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04407.x · Cited by 46 · see citing works
Centanni, S. W., Burnett, E. J., Trantham‐Davidson, H., & Chandler, L. J. (2016) · Addiction Biology · doi:10.1111/adb.12353 · Cited by 44 · see citing works
McMurray, M. S., Amodeo, L. R., & Roitman, J. D. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.288 · Cited by 40 · see citing works
Koskinen, S. M., Ahveninen, J., Kujala, T., Kaprio, J. A., O’Donnell, B. F., Osipova, D. V., Viken, R. J., Näätänen, R., & Rose, R. J. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01470.x · Cited by 29 · see citing works
Executive performance and dysexecutive symptoms in binge drinking adolescents
Hernández, S. G., & García‐Moreno, L. M. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.01.003 · Cited by 29 · see citing works
Seo, H., Seol, M.-J., & Lee, K. (2015) · Molecular Brain · doi:10.1186/s13041-015-0103-4 · Cited by 28 · see citing works
Schmidt, S. L., Dorsett, C. R., Iyengar, A. K., & Frӧhlich, F. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw242 · Cited by 24 · see citing works
Ethanol Enhances Human Hyperpolarization‐Activated Cyclic Nucleotide‐Gated Currents
Chen, Y., Wu, P., Fan, X., Chen, H., Yang, J., Song, T., & Huang, C. (2012) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2012.01826.x · Cited by 14 · see citing works
Working memory capacity and addiction treatment outcomes in adolescents
Houck, J. M., & Ewing, S. W. F. (2017) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2017.1344680 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Consequences of adolescent drug use
Steinfeld, M. R., & Torregrossa, M. M. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02590-4 · Cited by 237 · see citing works
“Recent studies have reported deficits in recall of an extinguished fear response [54], deficits in reversal learning [43], and impaired working memory [55, 56] following AAE.”
BackgroundAdolescent neurodevelopment and substance use: receptor expression and behavioral consequences
Thorpe, H. H. A., Hamidullah, S., Jenkins, B. W., & Khokhar, J. Y. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107431 · Cited by 97 · see citing works
Li, J., Wang, H., Liu, D., Li, X., He, L., Pan, J., Shen, Q., & Peng, Y. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.02.001 · Cited by 92 · see citing works
Varodayan, F. P., Pahng, A. R., Davis, T. D., Gandhi, P., Bajo, M., Steinman, M. Q., Kiosses, W. B., Blednov, Y. A., Burkart, M. D., Edwards, S., et al. (2023) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2023.02.020 · Cited by 50 · see citing works
Joffe, M. E., Winder, D. G., & Conn, P. J. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108126 · Cited by 52 · see citing works
Somatostatin neurons control an alcohol binge drinking prelimbic microcircuit in mice
Dao, N. C., Brockway, D. F., Nair, M. S., Sicher, A. R., & Crowley, N. A. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01050-1 · Cited by 53 · see citing works
Hughes, B. A., Crofton, E. J., O’Buckley, T. K., Herman, M. A., & Morrow, A. L. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107805 · Cited by 49 · see citing works
Ardinger, C. E., Lapish, C. C., Czachowski, C. L., & Grahame, N. J. (2022) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14924 · Cited by 45 · see citing works
Timme, N. M., Ma, B., Linsenbardt, D. N., Cornwell, E., Galbari, T., & Lapish, C. C. (2022) · Nature Communications · doi:10.1038/s41467-022-31731-4 · Cited by 38 · see citing works
Galaj, E., Guo, C., Huang, D., Ranaldi, R., & Ma, Y. (2020) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2020.108309 · Cited by 31 · see citing works
Cannady, R., Nimitvilai, S., Jennings, S. D., Woodward, J. J., & Mulholland, P. J. (2020) · eNeuro · doi:10.1523/eneuro.0077-20.2020 · Cited by 30 · see citing works
Animal Models of the Behavioral Symptoms of Substance Use DisordersPreprint
Vanderschuren, L. J. M. J., & Ahmed, S. H. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a040287 · Cited by 28 · see citing works
Hamidullah, S., Lutelmowski, C. D., Creighton, S. D., Luciani, K. R., Frie, J. A., Winters, B. D., & Khokhar, J. Y. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110141 · Cited by 28 · see citing works
Sergio, T. D. O., Frasier, R. M., & Hopf, F. W. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1116901 · Cited by 28 · see citing works
Flores‐Bonilla, A., Oliveira, B. D., Silva-Gotay, A., Lucier, K. W., & Richardson, H. N. (2021) · Biology of Sex Differences · doi:10.1186/s13293-021-00395-y · Cited by 27 · see citing works
Adolescent binge drinking leads to long-lasting changes in cortical microcircuits in mice
Sicher, A. R., Starnes, W. D., Griffith, K. R., Dao, N. C., Smith, G. C., Brockway, D. F., & Crowley, N. A. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109561 · Cited by 27 · see citing works
Seemiller, L. R., & Gould, T. J. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107234 · Cited by 23 · see citing works
Obray, J. D., Landin, J. D., Vaughan, D. T., Scofield, M. D., & Chandler, L. J. (2022) · Addiction Neuroscience · doi:10.1016/j.addicn.2022.100044 · Cited by 26 · see citing works
Schindler, A. G., Baskin, B. M., Juarez, B., Lee, S. J., Hendrickson, R. C., Pagulayan, K. F., Zweifel, L. S., Raskind, M. A., Phillips, P. E. M., Peskind, E. R., et al. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14605 · Cited by 26 · see citing works
Li, M., Cabrera-García, D., Salling, M. C., Au, E., Yang, G., & Harrison, N. L. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108501 · Cited by 24 · see citing works
Self-citationFalco, E. D., White, S., Morningstar, M. D., Ma, B., Nkurunziza, L. T., Ahmed‐Dilibe, A., Wellman, C. L., & Lapish, C. C. (2021) · Addiction Biology · doi:10.1111/adb.13004 · Cited by 23 · see citing works
Joffe, M. E., Winder, D. G., & Conn, P. J. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14546 · Cited by 21 · see citing works
Adolescent Alcohol and Stress Exposure Rewires Key Cortical Neurocircuitry
Sicher, A. R., Duerr, A., Starnes, W. D., & Crowley, N. A. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.896880 · Cited by 25 · see citing works
Koppensteiner, P., Galvin, C., & Ninan, I. (2019) · Synapse · doi:10.1002/syn.22090 · Cited by 21 · see citing works
Targeting prefrontal cortex GABAergic microcircuits for the treatment of alcohol use disorder
Fish, K. N., & Joffe, M. E. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.936911 · Cited by 20 · see citing works
Ferranti, A. S., Johnson, K. A., Winder, D. G., Conn, P. J., & Joffe, M. E. (2022) · Alcohol · doi:10.1016/j.alcohol.2022.02.003 · Cited by 19 · see citing works
Thompson, S. M., Fabian, C. B., Ferranti, A. S., & Joffe, M. E. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109638 · Cited by 19 · see citing works
Estrogen Modulates Ethanol‐Induced Memory Deficit in Postpubertal Adolescent Rats
Sircar, R. (2018) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13921 · Cited by 19 · see citing works
Sampedro‐Piquero, P., Moreno‐Fernández, R. D., Begega, A., López, M., & Santín, L. J. (2022) · Addiction Biology · doi:10.1111/adb.13158 · Cited by 19 · see citing works
Kipp, B. T., Nunes, P. T., Galaj, E., Hitchcock, B., Nasra, T., Poynor, K. R., Heide, S., Reitz, N. L., & Savage, L. M. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.08.014 · Cited by 18 · see citing works
Gómez‐A, A., Dannenhoffer, C. A., Elton, A., Lee, S., Ban, W., Shih, Y. I., Boettiger, C. A., & Robinson, D. L. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.778884 · Cited by 16 · see citing works
Blood Vessels as a Key Mediator for Ethanol Toxicity: Implication for Neuronal Damage
Nakayama, K., & Hasegawa, H. (2022) · Life · doi:10.3390/life12111882 · Cited by 17 · see citing works
Adolescence alcohol exposure impairs fear extinction and alters medial prefrontal cortex plasticity
Lawson, K., Scarlata, M. J., Cho, W. C., Mangan, C., Petersen, D., Thompson, H. M., Ehnstrom, S., Mousley, A. L., Bezek, J. L., & Bergstrom, H. C. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109048 · Cited by 16 · see citing works
Effect of ketamine on binge drinking patterns in crossed high alcohol-preferring (cHAP) mice
Ardinger, C. E., Winkler, G. A., Lapish, C. C., & Grahame, N. J. (2021) · Alcohol · doi:10.1016/j.alcohol.2021.09.004 · Cited by 16 · see citing works
Modeling Aversion Resistant Alcohol Intake in Indiana Alcohol-Preferring (P) Rats
Katner, S. N., Sentir, A. M., Steagall, K. B., Ding, Z., Wetherill, L. F., Hopf, F. W., & Engleman, E. A. (2022) · Brain Sciences · doi:10.3390/brainsci12081042 · Cited by 15 · see citing works
Domi, A., Cadeddu, D., Lucente, E., Gobbo, F., Edvardsson, C. E., Petrella, M., Jerlhag, E., Ericson, M., Söderpalm, B., & Adermark, L. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-01887-2 · Cited by 14 · see citing works
Sicher, A. R., Liss, A., Vozella, V., Marsland, P., Seemiller, L. R., Springer, M., Starnes, W. D., Griffith, K. R., Smith, G. C., Astefanous, A., et al. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100171 · Cited by 14 · see citing works
Allen, S. J., & Morishita, H. (2024) · Science Advances · doi:10.1126/sciadv.adh3920 · Cited by 13 · see citing works
de Oliveira, I. G., Queiroz, L. Y., da Silva, C. C. S., Cartágenes, S. D. C., Fernandes, L. M. P., de Souza-Júnior, F. J. C., Bittencourt, L. O., Lima, R. R., Martins, M. D., Schmidt, T. R., et al. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116316 · Cited by 12 · see citing works
Anton, P. E., Maphis, N. M., Linsenbardt, D. N., & Coleman, L. G. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-81908-7_10 · Cited by 12 · see citing works
Ardinger, C. E., Grahame, N. J., Lapish, C. C., & Linsenbardt, D. N. (2020) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14419 · Cited by 12 · see citing works
Hughes, B. A., O’Buckley, T. K., Boero, G., Herman, M. A., & Morrow, A. L. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01034-1 · Cited by 12 · see citing works
Joffe, M. E., Santiago, C. I., Vermudez, S. A. D., Fisher, N. M., Dogra, S., Niswender, C. M., & Conn, P. J. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01041-2 · Cited by 12 · see citing works
Matthews, D. B., Scaletty, S. J., Trapp, S., Kastner, A., Schneider, A., Schreiber, A. C., & Rossmann, G. L. (2022) · Brain Sciences · doi:10.3390/brainsci12050606 · Cited by 11 · see citing works
O’Herron, P. J., Summers, P. M., Shih, A. Y., Kara, P., & Woodward, J. J. (2019) · Alcohol · doi:10.1016/j.alcohol.2019.12.001 · Cited by 10 · see citing works
Areas of Convergence and Divergence in Adolescent Social Isolation and Binge Drinking: A Review
Lodha, J., Brocato, E. R., & Wolstenholme, J. T. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.859239 · Cited by 10 · see citing works
Frasier, R. M., Sergio, T. D. O., Starski, P. A., Grippo, A. J., & Hopf, F. W. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1244389 · Cited by 9 · see citing works
Short-term Montreal Cognitive Assessment predicts functional outcome after endovascular therapy
Zhang, M., Wang, K., Xie, L., & Pan, X. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.808415 · Cited by 11 · see citing works
Constitutive Genetic Deletion of Hcn1 Increases Alcohol Preference during Adolescence
Salling, M. C., & Harrison, N. L. (2020) · Brain Sciences · doi:10.3390/brainsci10110763 · Cited by 9 · see citing works
Self-citationDysfunctions of cellular context-sensitivity in neurodevelopmental learning disabilities
Granato, A., Phillips, W. A., Schulz, J. M., Mototaka Suzuki, A., & Larkum, M. E. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105688 · Cited by 8 · see citing works
Sergio, T. D. O., Darevsky, D. M., Kellner, J., Soares-Rachetti, V. D. P., Albino, M. D. C., Maulucci, D. P., Wean, S. E., & Hopf, F. W. (2024) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2024.111008 · Cited by 8 · see citing works
Obray, J. D., Wilkes, E. T., Scofield, M. D., & Chandler, L. J. (2024) · eLife · doi:10.7554/elife.101667 · Cited by 9 · see citing works
Kumar, J. S. D., Molotkov, A., Salling, M. C., Carberry, P., Prabhakaran, J., Castrillon, J., & Mintz, A. (2021) · Pharmacological Reports · doi:10.1007/s43440-021-00311-6 · Cited by 7 · see citing works
Self-citationTowner, T. T., Goyden, M. A., Coleman, H. J., Drumm, M. K., Ritchie, I. P., Lieb, K. R., Varlinskaya, E. I., & Werner, D. F. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109663 · Cited by 8 · see citing works
Luo, Y., Galaj, E., & Ma, Y. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24737 · Cited by 6 · see citing works
McNamara, T. A., Weng, H., Liao, H. Y., & Ito, R. (2025) · Scientific Reports · doi:10.1038/s41598-024-82517-1 · Cited by 5 · see citing works
Kalelkar, A., Sipe, G. O., Costa, A. R. C. E., Lorenzo, I. M., Nguyen, M., Linares-García, I., Vazey, E. M., & Huda, R. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109800 · Cited by 5 · see citing works
Fleites, V., Markwalter, P., Johnson, K., & Biasi, M. D. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.28.482336 · Cited by 4 · see citing works
Keum, D., & Medina, A. E. (2024) · Alcohol · doi:10.1016/j.alcohol.2024.02.006 · Cited by 3 · see citing works
Is tau pathology a relevant factor in neuronal damage induced by alcohol and other drugs?
Olesen, M. A., Ancía, A., & Quintanilla, R. A. (2025) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2025.168059 · Cited by 3 · see citing works
Chronic alcohol consumption alters sex-dependent BNST neuron function in rhesus macaques
Pleil, K. E., Grant, K. A., Carlson, V. C. C., & Kash, T. L. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100638 · Cited by 3 · see citing works
A Cross-Sectional Evaluation of Cigarette Smoking in the Brazilian Youth Population
de Brito, E. S., Bessel, M., Dornelles, T. M., Moreno, F. F., Pereira, G. F. M., & Wendland, E. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.614592 · Cited by 3 · see citing works
Buján, G. E., D’Alessio, L., Serra, H. A., Guelman, L. R., & Molina, S. J. (2024) · Neurotoxicity Research · doi:10.1007/s12640-024-00707-1 · Cited by 3 · see citing works
Voluntary alcohol consumption disrupts coupling of prefrontal cortical activity to arousalPreprint
Sipe, G. O., Linares-García, I., Nguyen, M. H., Vazey, E. M., & Huda, R. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.01.429229 · Cited by 3 · see citing works
Timme, N. M., Ma, B., Linsenbardt, D. N., Cornwell, E., Galbari, T., & Lapish, C. C. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.15.435169 · Cited by 3 · see citing works
Sergio, T. D. O., Darevsky, D. M., Soares, V. D. P., Albino, M. D. C., Maulucci, D. P., Wean, S. E., & Hopf, F. W. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.18.492488 · Cited by 3 · see citing works
Starski, P. A., Morningstar, M. D., Katner, S. N., Frasier, R. M., Sergio, T. D. O., Wean, S. E., Lapish, C. C., & Hopf, F. W. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.24.493243 · Cited by 3 · see citing works
de Brito, E. S., Bessel, M., Kops, N. L., Albrechet‐Souza, L., Moreno, F. F., Koskan, A. M., Dornelles, T. M., Pinheiro, B. H. G., Basgalupp, S. P., & Wendland, E. (2025) · Scientific Reports · doi:10.1038/s41598-025-31026-w · Cited by 2 · see citing works
Anterior cingulate cortex activation of claustrum projection neuron subtypes is enhanced by alcohol
Wulff, A. B., Sheats, S. H., Douglass, E. A., & Mathur, B. N. (2026) · Neuropharmacology · doi:10.1016/j.neuropharm.2026.110954 · Cited by 2 · see citing works
Licheri, V., Talani, G., Biggio, G., & Sanna, E. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109423 · Cited by 2 · see citing works
Obray, J. D., Wilkes, E. T., Scofield, M. D., & Chandler, L. J. (2025) · eLife · doi:10.7554/elife.101667.3 · Cited by 1 · see citing works
Mejía-Gómez, H., Fawcett‐Patel, J. M., Maxwell, F., Collins, G., Zakris, S. A., & Salling, M. C. (2026) · Neuropharmacology · doi:10.1016/j.neuropharm.2026.111015 · Cited by 1 · see citing works
Self-citationArce, C., Mira, R. G., Lira, M., & Cerpa, W. F. (2023) · Stresses · doi:10.3390/stresses4010001 · Cited by 1 · see citing works
Obray, J. D., Wilkes, E. T., Scofield, M. D., & Chandler, L. J. (2024) · eLife · doi:10.7554/elife.101667.1 · Cited by 1 · see citing works
Persistent “Sag” in Prefrontal Cortex Function following Adolescent Binge Drinking
Joffe, M. E. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1755-18.2018
Zlateva, S., Marinov, P., & Bonchev, G. (2021) · Journal of IMAB - Annual Proceeding (Scientific Papers) · doi:10.5272/jimab.2021271.3502
Comparison of factor analysis models applied to the NCANDA neuropsychological test battery
Cummins, K. M., Pitpitan, E. V., Brumback, T., Moore, T. M., Trim, R. S., Clark, D. B., Brown, S. A., & Tapert, S. F. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263174
Olesen, M. A., & Quintanilla, R. A. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-89834-8.00043-x · Cited by 1 · see citing works
Buján, G. E., D’Alessio, L., Serra, H. A., Guelman, L. R., & Molina, S. J. (2023) · Research Square · doi:10.21203/rs.3.rs-3754611/v1
Hughes, B. A., O’Buckley, T. K., Boero, G., & Morrow, A. L. (2024) · Alcohol · doi:10.1016/j.alcohol.2024.07.005
Buján, G. E., Corsi, G. N., D'Alessio, L., Serra, H. A., Molina, S. J., & Guelman, L. R. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.5059896
Adolescent Alcohol Exposure Dysregulates Developing Cortical GABA Circuits
Sicher, A. R., & Crowley, N. A. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-81908-7_8
Obray, J. D., Wilkes, E. T., Scofield, M. D., & Chandler, L. J. (2025) · eLife · doi:10.7554/elife.101667.2
Adolescent alcohol exposure disrupts retrosplenial cortex physiology in adult malesPreprint
Taxier, L. R., Kooyman, L. S., Markowitz, S., Wojick, J. A., & Kash, T. L. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.29.679287
Buján, G. E., D’Alessio, L., Serra, H. A., Corsi, G. N., Molina, S. J., & Guelman, L. R. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70279
A mixed model of adolescent alcohol exposure reveals divergent behavioral and neural outcomes
DeMatteo, M. C., Gakare, S. G., Griffith, M., Ha, L., Maxwell, F., Mejía-Gómez, H., & Salling, M. C. (2026) · Physiology & Behavior · doi:10.1016/j.physbeh.2026.115472
Self-citationCirafesi, C. K., Karkhanis, A. N., & Diaz, M. R. (2026) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2026.111887
Qian, G., Jarrell, H., Maxwell, F., Mejía-Gómez, H., & Salling, M. C. (2026) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.70415
Self-citation
- Authors
- Salling, M. C., Skelly, M. J., Avegno, E., Regan, S., Zeric, T., Nichols, E., & Harrison, N. L.
- Affiliations
- Columbia University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-06-18
- Volume
- 38
- Issue
- 27
- Pages
- 6207-6222
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6031577
- OpenAlex
- W2808738602
- Cited by
- 89
- References
- 81
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 13 · 2023: 13 · 2022: 18 · 2021: 16 · 2020: 9 · 2019: 4 · 2018: 2
- FWCI
- 3.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (2t32gm008464-31, 5f32aa022028-02)
- National Institute on Alcohol Abuse and Alcoholism (F32 AA-022028, R01AA023531)
- National Institute of General Medical Sciences (T32 GM-008464)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- adolescent binge drinking, alcohol consumption, prefrontal cortex, hyperpolarization-activated current, intrinsic excitability, working memory deficits, persistent activity, resting membrane potential, pyramidal neurons, prelimbic cortex, alcohol use disorder risk
- MeSH terms
- Action Potentials, Ethanol, Animals, Central Nervous System Depressants, Disease Models, Animal, Male, Memory, Short-Term, Mice, Inbred C57BL, Prefrontal Cortex, Pyramidal Cells, Mice, Binge Drinking
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review