Abstract
Problem alcohol drinking remains an enormous personal, social, and clinical challenge, and compulsion-like drinking (intake despite known negative consequences) can strongly contribute. Here we describe the lickometry method, a simple procedure (determining lick times) but, by analyzing many aspects of licking (or some other behavior), but with potential to provide important insights into underlying psychological and action strategies. We compare compulsion-like drinking with moderate challenge or higher challenge (ModChD or HiChD, quinine-alcohol) versus alcohol-only drinking (AOD). Classic studies suggest two main strategies during oral intake, more bouts of licking (indicating higher motivation), or longer (often faster) bouts (indicating higher palatability). In strong contrast, ModChD shows decreased variability of many lick measures, from lick speed to tongue shape, consistent with importance of automaticity in addiction. Further, and surprisingly, HiChD retains decreased tongue variability (and earlier bout start) seen with ModChD-versus-AOD, along with greatly disrupted intake. We relate these changes to regions of the Salience Network, which identifies and responds to important events. HiChD collapses mirrors inhibiting dorsal-medial prefrontal cortex (dMPF), while anterior insula cortex (AIC/ventral-frontal cortex) is linked to main value-driven action plan and also oral consumption. While AIC-dMPF likely work together, we find a novel dissociation in AIC-versus-dMPF function: AIC provides overall drive and firm commitment regardless of challenge level, while dMPF organizes action across time, but the battle for acting is won or lost in the dMPF.
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References
Rudisch DM, Krasko MN, Nisbet AF et al (2022) Assays of tongue force, timing, and dynamics in rat and mouse models. Brain Res Bull 185:49–55
CDC (2014) Excessive drinking costs U.S. $223.5 billion. Center for Disease Control, Atlanta
Bouchery EE, Harwood HJ, Sacks JJ et al (2011) Economic costs of excessive alcohol consumption in the U.S., 2006. Am J Prev Med 41:516–524
Sacks JJ, Roeber J, Bouchery EE et al (2013) State costs of excessive alcohol consumption, 2006. Am J Prev Med 45:474–485
SAMHSA (2014) Risk and protective factors and initiation of substance use: results from the 2014 national survey on drug use and health. Substance Abuse and Mental Health Services Administration
WHO (2014) Global status report on alcohol and health-2014. World Health Organization
Dawson DA, Grant BF, Li TK (2005) Quantifying the risks associated with exceeding recommended drinking limits. Alcohol Clin Exp Res 29:902–908
Moos RH, Moos BS (2006) Rates and predictors of relapse after natural and treated remission from alcohol use disorders. Addiction 101:212–222
Rehm J, Mathers C, Popova S et al (2009) Global burden of disease and injury and economic cost attributable to alcohol use and alcohol-use disorders. Lancet 373:2223–2233
Grant BF, Chou SP, Saha TD et al (2017) Prevalence of 12-month alcohol use, high-risk drinking, and DSM-IV alcohol use disorder in the United States, 2001-2002 to 2012-2013: results from the national epidemiologic survey on alcohol and related conditions. JAMA Psychiatry 74:911–923
Carvalho AF, Heilig M, Perez A et al (2019) Alcohol use disorders. Lancet 394:781–792
White A, Castle IJ, Chen CM et al (2015) Converging patterns of alcohol use and related outcomes among females and males in the United States, 2002 to 2012. Alcohol Clin Exp Res 39:1712–1726
Erol A, Karpyak VM (2015) Sex and gender-related differences in alcohol use and its consequences: contemporary knowledge and future research considerations. Drug Alcohol Depend 156:1–13
Brady KT, Randall CL (1999) Gender differences in substance use disorders. Psychiatr Clin North Am 22:241–252
Becker JB, Koob GF (2016) Sex differences in animal models: focus on addiction. Pharmacol Rev 68:242–263
Larimer ME, Palmer RS, Marlatt GA (1999) Relapse prevention. An overview of Marlatt’s cognitive-behavioral model. Alcohol Res Health 23:151–160
Anton RF (2000) Obsessive-compulsive aspects of craving: development of the obsessive compulsive drinking scale. Addiction 95(Suppl 2):S211–S217
Sinha R (2009) Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict Biol 14:84–98
Tiffany ST, Conklin CA (2000) A cognitive processing model of alcohol craving and compulsive alcohol use. Addiction 95(Suppl 2):S145–S153
Epstein DH, Kowalczyk WJ (2018) Compulsive seekers: our take. Two clinicians’ perspective on a new animal model of addiction. Neuropsychopharmacology 43:677–679
Giuliano C, Pena-Oliver Y, Goodlett CR et al (2018) Evidence for a long-lasting compulsive alcohol seeking phenotype in rats. Neuropsychopharmacology 43:728–738
Everitt BJ, Robbins TW (2016) Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol 67:23–50
Hopf FW (2017) Do specific NMDA receptor subunits act as gateways for addictive behaviors? Genes Brain Behav 16:118–138
Hopf FW, Lesscher HM (2014) Rodent models for compulsive alcohol intake. Alcohol 48:253–264
Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238
Kranzler HR, Soyka M (2018) Diagnosis and pharmacotherapy of alcohol use disorder: a review. JAMA 320:815–824
Spanagel R (2009) Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol Rev 89:649–705
Mann K, Roos CR, Hoffmann S et al (2018) Precision medicine in alcohol dependence: a controlled trial testing pharmacotherapy response among reward and relief drinking phenotypes. Neuropsychopharmacology 43:891–899
Flores-Bonilla A, Richardson HN (2020) Sex differences in the neurobiology of alcohol use disorder. Alcohol Res 40:04
Guinle MIB, Sinha R (2020) The role of stress, trauma, and negative affect in alcohol misuse and alcohol use disorder in women. Alcohol Res 40:05
Altemus M, Sarvaiya N, Neill Epperson C (2014) Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol 35:320–330
Filkowski MM, Olsen RM, Duda B et al (2017) Sex differences in emotional perception: meta analysis of divergent activation. NeuroImage 147:925–933
Centanni SW, Janes AC, Haggerty DL et al (2021) Better living through understanding the insula: why subregions can make all the difference. Neuropharmacology 198:108765
Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356
Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci USA 105:12569–12574
Craig AD (2010) Once an island, now the focus of attention. Brain Struct Funct 214:395–396
Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667
Kolling N, Scholl J, Chekroud A et al (2018) Prospection, perseverance, and insight in sequential behavior. Neuron 99:1069–1082 e7
Namkung H, Kim SH, Sawa A (2018) The insula: an underestimated brain area in clinical neuroscience, psychiatry, and neurology: (trends in neuroscience 40, 200-207, 2017). Trends Neurosci 41:551–554
Ochi R, Fujita N, Goto N et al (2021) Medial prefrontal area reductions, altered expressions of cholecystokinin, parvalbumin, and activating transcription factor 4 in the corticolimbic system, and altered emotional behavior in a progressive rat model of type 2 diabetes. PLoS One 16:e0256655
Yamashita PS, Spiacci A Jr, Hassel JE Jr et al (2017) Disinhibition of the rat prelimbic cortex promotes serotonergic activation of the dorsal raphe nucleus and panicolytic-like behavioral effects. J Psychopharmacol 31:704–714
Seif T, Chang SJ, Simms JA et al (2013) Cortical activation of accumbens hyperpolarization-active NMDARs mediates aversion-resistant alcohol intake. Nat Neurosci 16:1094–1100
De Oliveira Sergio T, Lei K, Kwok C et al (2021) The role of anterior insula-brainstem projections and alpha-1 noradrenergic receptors for compulsion-like and alcohol-only drinking. Neuropsychopharmacology. 35:1751–1760
Chen NM, Lasek AM (2020) Perineuronal nets in the insula regulate aversion-resistant alcohol drinking. Addict Biol. 25:e12821
Arcurio LR, Finn PR, James TW (2015) Neural mechanisms of high-risk decisions-to-drink in alcohol-dependent women. Addict Biol 20:390–406
Grodin EN, Sussman L, Sundby K et al (2018) Neural correlates of compulsive alcohol seeking in heavy drinkers. Biol Psych Cogn Neuro Neuroimag 2:1022–1031
Myrick H, Anton RF, Li X et al (2004) Differential brain activity in alcoholics and social drinkers to alcohol cues: relationship to craving. Neuropsychopharmacology 29:393–402
Claus ED, Ewing SW, Filbey FM et al (2011) Identifying neurobiological phenotypes associated with alcohol use disorder severity. Neuropsychopharmacology 36:2086–2096
Chester DS, Lynam DR, Milich R et al (2016) How do negative emotions impair self-control? A neural model of negative urgency. NeuroImage 132:43–50
Seo D, Jia Z, Lacadie CM et al (2011) Sex differences in neural responses to stress and alcohol context cues. Hum Brain Mapp 32:1998–2013
Dager AD, Anderson BM, Rosen R et al (2014) Functional magnetic resonance imaging (fMRI) response to alcohol pictures predicts subsequent transition to heavy drinking in college students. Addiction 109:585–595
Lim AC, Cservenka A, Ray LA (2017) Effects of alcohol dependence severity on neural correlates of delay discounting. Alcohol Alcohol 52:506–515
Weafer J, Gorka SM, Dzemidzic M et al (2021) Neural correlates of inhibitory control are associated with stimulant-like effects of alcohol. Neuropsychopharmacology 46:1442–1450
Srivastava AB, Sanchez-Pena J, Levin FR et al (2021) Drinking reduction during cognitive behavioral therapy for alcohol use disorder is associated with a reduction in anterior insula-bed nucleus of the stria terminalis resting-state functional connectivity. Alcohol Clin Exp Res 45:1596–1606
Morley KC, Logge WB, Fraser I et al (2021) High-dose baclofen attenuates insula activation during anticipatory anxiety in treatment-seeking alcohol dependant individuals: preliminary findings from a pharmaco-fMRI study. Eur Neuropsychopharmacol 46:28–36
Wegner SA, Hu B, De Oliveira Sergio T et al (2019) A novel NMDA receptor-based intervention to suppress compulsion-like alcohol drinking. Neuropharmacology 157:107681
Radke AK, Sneddon EA, Frasier RM et al (2021) Recent perspectives on sex differences in compulsion-like and binge alcohol drinking. Int J Mol Sci 22
McGuire JT, Botvinick MM (2010) Prefrontal cortex, cognitive control, and the registration of decision costs. Proc Natl Acad Sci USA 107:7922–7926
Jansma JM, Ramsey NF, de Zwart JA et al (2007) fMRI study of effort and information processing in a working memory task. Hum Brain Mapp 28:431–440
Hayden BY, Pearson JM, Platt ML (2011) Neuronal basis of sequential foraging decisions in a patchy environment. Nat Neurosci 14:933–939
Sterzer P, Kleinschmidt A (2010) Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 214:611–622
Hillman KL, Bilkey DK (2013) Persisting through subjective effort: a key role for the anterior cingulate cortex? Behav Brain Sci 36(691–2):707–726
Kolling N, Wittmann M, Rushworth MFS (2014) Multiple neural mechanisms of decision making and their competition under changing risk pressure. Neuron 81:1190–1202
Daniel ML, Cocker PJ, Lacoste J et al (2017) The anterior insula bidirectionally modulates cost-benefit decision-making on a rodent gambling task. Eur J Neurosci 46:2620–2628
Wang Y, Liu Y, Yang L et al (2015) Novelty seeking is related to individual risk preference and brain activation associated with risk prediction during decision making. Sci Rep 5:10534
Jenni NL, Larkin JD, Floresco SB (2017) Prefrontal dopamine D1 and D2 receptors regulate dissociable aspects of decision making via distinct ventral striatal and Amygdalar circuits. J Neurosci 37:6200–6213
Meder D, Haagensen BN, Hulme O et al (2016) Tuning the brake while raising the stake: network dynamics during sequential decision-making. J Neurosci 36:5417–5426
van der Laan LN, de Ridder DT, Charbonnier L et al (2014) Sweet lies: neural, visual, and behavioral measures reveal a lack of self-control conflict during food choice in weight-concerned women. Front Behav Neurosci 8:184
Frankenstein UN, Richter W, McIntyre MC et al (2001) Distraction modulates anterior cingulate gyrus activations during the cold pressor test. NeuroImage 14:827–836
Zeng Y, Hu D, Yang W et al (2018) A voxel-based analysis of neurobiological mechanisms in placebo analgesia in rats. NeuroImage 178:602–612
Kaplan JT, Gimbel SI, Harris S (2016) Neural correlates of maintaining one’s political beliefs in the face of counterevidence. Sci Rep 6:39589
Aimone JA, Houser D, Weber B (2014) Neural signatures of betrayal aversion: an fMRI study of trust. Proc Biol Sci 281:20132127
Benoit RG, Gilbert SJ, Burgess PW (2011) A neural mechanism mediating the impact of episodic prospection on farsighted decisions. J Neurosci 31:6771–6779
Nelson SM, Dosenbach NU, Cohen AL et al (2010) Role of the anterior insula in task-level control and focal attention. Brain Struct Funct 214:669–680
Stoppel CM, Boehler CN, Strumpf H et al (2011) Neural processing of reward magnitude under varying attentional demands. Brain Res 1383:218–229
Grupe DW, Oathes DJ, Nitschke JB (2013) Dissecting the anticipation of aversion reveals dissociable neural networks. Cereb Cortex 23:1874–1883
Sadaghiani S, D’Esposito M (2015) Functional characterization of the Cingulo-Opercular network in the maintenance of tonic alertness. Cereb Cortex 25:2763–2773
Darevsky D, Gill TM, Vitale KR et al (2019) Drinking despite adversity: behavioral evidence for a head down and push strategy of conflict-resistant alcohol drinking in rats. Addict Biol 24:426–437
Darevsky D, Hopf FW (2020) Behavioral indicators of succeeding and failing under higher-challenge compulsion-like alcohol drinking in rat. Behav Brain Res 393:112768
De Oliveira Sergio T, Darevsky D, de Paula Soares V, de Cassia Albino M, Maulucci D, Wean S, Hopf FW Evidence for different greater-persistence strategies under lower and higher challenge for alcohol in female rats. Biorvix:www.biorxiv.org/content/10.1101/2022.05.18.492488v1
Starski P, Morningstar M, Katner S, Frasier R, De Oliveira Sergio T, Wean S, Lapish C, Hopf FW Anterior insular cortex firing links initial and sustained encoding during aversion-resistant alcohol consumption. Biorvix. https://doi.org/10.1101/2022.05.24.493243
Ottenheimer D, Richard JM, Janak PH (2018) Ventral pallidum encodes relative reward value earlier and more robustly than nucleus accumbens. Nat Commun 9:4350
Bari BA, Grossman CD, Lubin EE et al (2019) Stable representations of decision variables for flexible behavior. Neuron 103:922–933 e7
Mukherjee N, Wachutka J, Katz DB (2019) Impact of precisely-timed inhibition of gustatory cortex on taste behavior depends on single-trial ensemble dynamics. elife 8:e45968
Sadacca BF, Mukherjee N, Vladusich T et al (2016) The behavioral relevance of cortical neural ensemble responses emerges suddenly. J Neurosci 36:655–669
Roebber JK, Izenwasser S, Chaudhari N (2015) Cocaine decreases saccharin preference without altering sweet taste sensitivity. Pharmacol Biochem Behav 133:18–24
Moore JD, Kleinfeld D, Wang F (2014) How the brainstem controls orofacial behaviors comprised of rhythmic actions. Trends Neurosci 37:370–380
Seif T, Simms JA, Lei K et al (2015) D-Serine and D-Cycloserine reduce compulsive alcohol intake in rats. Neuropsychopharmacology 40:2357–2367
Davis JD, Smith GP (1992) Analysis of the microstructure of the rhythmic tongue movements of rats ingesting maltose and sucrose solutions. Behav Neurosci 106:217–228
Patwell R, Yang H, Pandey SC et al (2021) An operant ethanol self-administration paradigm that discriminates between appetitive and consummatory behaviors reveals distinct behavioral phenotypes in commonly used rat strains. Neuropharmacology 201:108836
Lardeux S, Kim JJ, Nicola SM (2013) Intermittent access to sweet high-fat liquid induces increased palatability and motivation to consume in a rat model of binge consumption. Physiol Behav 114–115:21–31
Spector AC, Klumpp PA, Kaplan JM (1998) Analytical issues in the evaluation of food deprivation and sucrose concentration effects on the microstructure of licking behavior in the rat. Behav Neurosci 112:678–694
Naneix F, Peters KZ, McCutcheon JE (2020) Investigating the effect of physiological need states on palatability and motivation using microstructural analysis of licking. Neuroscience 447:155–166
Samson HH (2000) The microstructure of ethanol drinking: genetic and behavioral factors in the control of drinking patterns. Addiction 95(Suppl 2):S61–S72
Barkley-Levenson AM, Crabbe JC (2015) Distinct ethanol drinking microstructures in two replicate lines of mice selected for drinking to intoxication. Genes Brain Behav 14:398–410
Haggerty DL, Munoz B, Pennington T et al (2022) The role of anterior insular cortex inputs to dorsolateral striatum in binge alcohol drinking. elife 11:e77411
Davis JD, Perez MC (1993) Food deprivation- and palatability-induced microstructural changes in ingestive behavior. Am J Phys 264:R97–R103
Hopf FW, Chang SJ, Sparta DR et al (2010) Motivation for alcohol becomes resistant to quinine adulteration after 3 to 4 months of intermittent alcohol self-administration. Alcohol Clin Exp Res 34:1565–1573
Hsiao S, Fan RJ (1993) Additivity of taste-specific effects of sucrose and quinine: microstructural analysis of ingestive behavior in rats. Behav Neurosci 107:317–326
Baird JP, St John SJ, Nguyen EA (2005) Temporal and qualitative dynamics of conditioned taste aversion processing: combined generalization testing and licking microstructure analysis. Behav Neurosci 119:983–1003
Renteria R, Cazares C, Gremel CM (2020) Habitual ethanol seeking and licking microstructure of enhanced ethanol self-administration in ethanol-dependent mice. Alcohol Clin Exp Res 44:880–891
Flores-Bonilla A, De Oliveira B, Silva-Gotay A et al (2021) Shortening time for access to alcohol drives up front-loading behavior, bringing consumption in male rats to the level of females. Biol Sex Differ 12:51
Baker EJ, Farro J, Gonzales S et al (2014) Chronic alcohol self-administration in monkeys shows long-term quantity/frequency categorical stability. Alcohol Clin Exp Res 38:2835–2843
Gowin JL, Sloan ME, Stangl BL et al (2017) Vulnerability for alcohol use disorder and rate of alcohol consumption. Am J Psychiatry 174:1094–1101
Robinson SL, McCool BA (2015) Microstructural analysis of rat ethanol and water drinking patterns using a modified operant self-administration model. Physiol Behav 149:119–130
Parent MA, Amarante LM, Swanson K et al (2015b) Cholinergic and ghrelinergic receptors and KCNQ channels in the medial PFC regulate the expression of palatability. Front Behav Neurosci 9:284
Patton MS, Heckman M, Kim C et al (2021) Compulsive alcohol consumption is regulated by dorsal striatum fast-spiking interneurons. Neuropsychopharmacology 46:351–359
Gutierrez R, Carmena JM, Nicolelis MA et al (2006) Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J Neurophysiol 95:119–133
Baird JP, Choe A, Loveland JL et al (2009) Orexin-a hyperphagia: hindbrain participation in consummatory feeding responses. Endocrinology 150:1202–1216
Voon V, Derbyshire K, Ruck C et al (2015) Disorders of compulsivity: a common bias towards learning habits. Mol Psychiatry 20:345–352
Ersche KD, Lim TV, Ward LHE et al (2017) Creature of habit: a self-report measure of habitual routines and automatic tendencies in everyday life. Pers Individ Dif 116:73–85
Han SW, Eaton HP, Marois R (2019) Functional fractionation of the Cingulo-Opercular network: alerting insula and updating cingulate. Cereb Cortex 29:2624–2638
Craig AD (2009) How do you feel – now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70
Jaramillo AA, Randall PA, Stewart S et al (2018b) Functional role for cortical-striatal circuitry in modulating alcohol self-administration. Neuropharmacology 130:42–53
Dao NC, Brockway DF, Suresh Nair M et al (2021) Somatostatin neurons control an alcohol binge drinking prelimbic microcircuit in mice. Neuropsychopharmacology 46:1906–1917
Timme NM, Ma B, Linsenbardt D et al (2022) Compulsive alcohol drinking in rodents is associated with altered representations of behavioral control and seeking in dorsal medial prefrontal cortex. Nat Commun 13:3990
Hamilton DA, Barto D, Rodriguez CI et al (2014) Effects of moderate prenatal ethanol exposure and age on social behavior, spatial response perseveration errors and motor behavior. Behav Brain Res 269:44–54
Whishaw IQ, Tompkins GJ (1988) An optic-fiber photocell detector for measuring tongue protrusion in the rat: evaluation of recovery from localized cortical lesions. Physiol Behav 43:397–401
Whishaw IQ, Kolb B (1983) “Stick out your tongue”: tongue protrusion in neocortex and hypothalamic damaged rats. Physiol Behav 30:471–480
Castro AJ (1972) The effects of cortical ablations on tongue usage in the rat. Brain Res 45:251–253
Brimley CC, Mogenson GJ (1979) Oral motor deficits following lesions of the central nervous system in the rat. Am J Phys 237:R126–R131
Shipley JE, Rowland N, Antelman SM (1980) Orbital or medial frontal cortical lesions have different effects on tail pressure-elicited oral behaviors in rats. Physiol Behav 24:1091–1094
Parent MA, Amarante LM, Liu B et al (2015a) The medial prefrontal cortex is crucial for the maintenance of persistent licking and the expression of incentive contrast. Front Integr Neurosci 9:23
Horst NK, Laubach M (2009) The role of rat dorsomedial prefrontal cortex in spatial working memory. Neuroscience 164:444–456
Narayanan NS, Horst NK, Laubach M (2006) Reversible inactivations of rat medial prefrontal cortex impair the ability to wait for a stimulus. Neuroscience 139:865–876
Krigolson O, Bell J, Kent CM et al (2012) Reduced cortical motor potentials underlie reductions in memory-guided reaching performance. Mot Control 16:353–370
Smith NJ, Horst NK, Liu B et al (2010) Reversible inactivation of rat premotor cortex impairs temporal preparation, but not inhibitory control, during simple reaction-time performance. Front Integr Neurosci 4:124
Afonso VM, Sison M, Lovic V et al (2007) Medial prefrontal cortex lesions in the female rat affect sexual and maternal behavior and their sequential organization. Behav Neurosci 121:515–526
Horst NK, Laubach M (2013) Reward-related activity in the medial prefrontal cortex is driven by consumption. Front Neurosci 7:56
Stuss DT, Murphy KJ, Binns MA et al (2003) Staying on the job: the frontal lobes control individual performance variability. Brain 126:2363–2380
Stuss DT, Alexander MP, Shallice T et al (2005) Multiple frontal systems controlling response speed. Neuropsychologia 43:396–417
Croxson PL, Walton ME, O’Reilly JX et al (2009) Effort-based cost-benefit valuation and the human brain. J Neurosci 29:4531–4541
Simon NW, Wood J, Moghaddam B (2015) Action-outcome relationships are represented differently by medial prefrontal and orbitofrontal cortex neurons during action execution. J Neurophysiol 114:3374–3385
Rudebeck PH, Walton ME, Smyth AN et al (2006) Separate neural pathways process different decision costs. Nat Neurosci 9:1161–1168
Rich EL, Wallis JD (2016) Decoding subjective decisions from orbitofrontal cortex. Nat Neurosci 19:973–980
Sharpe MJ, Killcross S (2015) The prelimbic cortex directs attention toward predictive cues during fear learning. Learn Mem 22:289–293
Park J, Moghaddam B (2017) Impact of anxiety on prefrontal cortex encoding of cognitive flexibility. Neuroscience 345:193–202
Park J, Wood J, Bondi C et al (2016) Anxiety evokes hypofrontality and disrupts rule-relevant encoding by dorsomedial prefrontal cortex neurons. J Neurosci 36:3322–3335
Uddin LQ, Nomi JS, Hebert-Seropian B et al (2017) Structure and function of the human insula. J Clin Neurophysiol 34:300–306
Hayes DJ, Duncan NW, Xu J et al (2014) A comparison of neural responses to appetitive and aversive stimuli in humans and other mammals. Neurosci Biobehav Rev 45:350–368
Hauser TU, Eldar E, Dolan RJ (2017) Separate mesocortical and mesolimbic pathways encode effort and reward learning signals. Proc Natl Acad Sci USA 114:E7395–E7404
Ryman SG, El Shaikh AA, Shaff NA et al (2018) Proactive and reactive cognitive control rely on flexible use of the ventrolateral prefrontal cortex. Hum Brain Mapp 40:955–966
Hardung S, Epple R, Jackel Z et al (2017) A functional gradient in the rodent prefrontal cortex supports behavioral inhibition. Curr Biol 27:549–555
Chua HF, Gonzalez R, Taylor SF et al (2009) Decision-related loss: regret and disappointment. NeuroImage 47:2031–2040
Burke CJ, Tobler PN (2011) Reward skewness coding in the insula independent of probability and loss. J Neurophysiol 106:2415–2422
Kolling N, Behrens TE, Mars RB et al (2012) Neural mechanisms of foraging. Science 336:95–98
Dosenbach NU, Visscher KM, Palmer ED et al (2006) A core system for the implementation of task sets. Neuron 50:799–812
Wittmann MK, Fouragnan E, Folloni D et al (2020) Global reward state affects learning and activity in raphe nucleus and anterior insula in monkeys. Nat Commun 11:3771
Guillem K, Kravitz AV, Moorman DE et al (2010) Orbitofrontal and insular cortex: neural responses to cocaine-associated cues and cocaine self-administration. Synapse 64:1–13
DeCoteau WE, Kesner RP, Williams JM (1997) Short-term memory for food reward magnitude: the role of the prefrontal cortex. Behav Brain Res 88:239–249
Pribut HJ, Vazquez D, Brockett AT et al (2021) Prior cocaine exposure increases firing to immediate reward while attenuating cue and context signals related to reward value in the insula. J Neurosci 41:4667–4677
Laubach M, Caetano MS, Narayanan NS (2015) Mistakes were made: neural mechanisms for the adaptive control of action initiation by the medial prefrontal cortex. J Physiol 109:104–117
Ito S, Ogawa H (1994) Neural activities in the fronto-opercular cortex of macaque monkeys during tasting and mastication. Jpn J Physiol 44:141–156
Petyko Z, Galosi R, Toth A et al (2015) Responses of rat medial prefrontal cortical neurons to Pavlovian conditioned stimuli and to delivery of appetitive reward. Behav Brain Res 287:109–119
Amarante LM, Caetano MS, Laubach M (2017) Medial frontal theta is entrained to rewarded actions. J Neurosci 37:10757–10769
Yaxley S, Rolls ET, Sienkiewicz ZJ (1988) The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiol Behav 42:223–229
Hollander JA, Lu Q, Cameron MD et al (2008) Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105:19480–19485
Pelloux Y, Murray JE, Everitt BJ (2013) Differential roles of the prefrontal cortical subregions and basolateral amygdala in compulsive cocaine seeking and relapse after voluntary abstinence in rats. Eur J Neurosci 38:3018–3026
Rotge JY, Cocker PJ, Daniel ML et al (2017) Bidirectional regulation over the development and expression of loss of control over cocaine intake by the anterior insula. Psychopharmacology 234:1623–1631
Baldo BA, Spencer RC, Sadeghian K et al (2016) GABA-mediated inactivation of medial prefrontal and agranular insular cortex in the rat: contrasting effects on hunger- and palatability-driven feeding. Neuropsychopharmacology 41:960–970
Pushparaj A, Le Foll B (2015) Involvement of the caudal granular insular cortex in alcohol self-administration in rats. Behav Brain Res 293:203–207
Jasmin L, Burkey AR, Granato A et al (2004) Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J Comp Neurol 468:425–440
Halcomb ME, Chumin EJ, Goni J et al (2019) Aberrations of anterior insular cortex functional connectivity in nontreatment-seeking alcoholics. Psychiatry Res Neuroimaging 284:21–28
Tan Y, Yan R, Gao Y et al (2022) Spatial-topographic nestedness of interoceptive regions within the networks of decision making and emotion regulation: combining ALE meta-analysis and MACM analysis. NeuroImage 260:119500
Porges EC, Decety J (2013) Violence as a source of pleasure or displeasure is associated with specific functional connectivity with the nucleus accumbens. Front Hum Neurosci 7:447
Poeppl TB, Nitschke J, Dombert B et al (2011) Functional cortical and subcortical abnormalities in pedophilia: a combined study using a choice reaction time task and fMRI. J Sex Med 8:1660–1674
Kesner RP, Gilbert PE (2007) The role of the agranular insular cortex in anticipation of reward contrast. Neurobiol Learn Mem 88:82–86
Smith KS, Graybiel AM (2013) A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron 79:361–374
Jezzini A, Caruana F, Stoianov I et al (2012) Functional organization of the insula and inner perisylvian regions. Proc Natl Acad Sci USA 109:10077–10082
Stapleton JR, Lavine ML, Wolpert RL et al (2006) Rapid taste responses in the gustatory cortex during licking. J Neurosci 26:4126–4138
Haaranen M, Scuppa G, Tambalo S et al (2020b) Anterior insula stimulation suppresses appetitive behavior while inducing forebrain activation in alcohol-preferring rats. Transl Psychiatry 10:150
Pushparaj A, Kim AS, Musiol M et al (2015) Differential involvement of the agranular vs granular insular cortex in the acquisition and performance of choice behavior in a rodent gambling task. Neuropsychopharmacology 40:2832–2842
Arguello AA, Wang R, Lyons CM et al (2017) Role of the agranular insular cortex in contextual control over cocaine-seeking behavior in rats. Psychopharmacology 234:2431–2441
Mendez-Ruette M, Linsambarth S, Moraga-Amaro R et al (2019) The role of the rodent insula in anxiety. Front Physiol 10:330
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Sergio, T.D.O., Starski, P.A., Hopf, F.W. (2023). Lickometry to Circuitry: How Compulsion-Like Alcohol Drinking Microstructure Helped Discover Functional Differences in Salience Network Regions. In: Cyders, M.A. (eds) Translational Research Methods for Alcohol Use Disorders. Neuromethods, vol 201. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3267-3_4
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DOI: https://doi.org/10.1007/978-1-0716-3267-3_4
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Publisher Name: Humana, New York, NY
Print ISBN: 978-1-0716-3266-6
Online ISBN: 978-1-0716-3267-3
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