Skip to main content

Lickometry to Circuitry: How Compulsion-Like Alcohol Drinking Microstructure Helped Discover Functional Differences in Salience Network Regions

  • Protocol
  • First Online:
Translational Research Methods for Alcohol Use Disorders

Part of the book series: Neuromethods ((NM,volume 201))

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. 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

    Article  PubMed  Google Scholar 

  2. CDC (2014) Excessive drinking costs U.S. $223.5 billion. Center for Disease Control, Atlanta

    Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. Sacks JJ, Roeber J, Bouchery EE et al (2013) State costs of excessive alcohol consumption, 2006. Am J Prev Med 45:474–485

    Article  PubMed  Google Scholar 

  5. 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

    Google Scholar 

  6. WHO (2014) Global status report on alcohol and health-2014. World Health Organization

    Google Scholar 

  7. Dawson DA, Grant BF, Li TK (2005) Quantifying the risks associated with exceeding recommended drinking limits. Alcohol Clin Exp Res 29:902–908

    Article  PubMed  Google Scholar 

  8. Moos RH, Moos BS (2006) Rates and predictors of relapse after natural and treated remission from alcohol use disorders. Addiction 101:212–222

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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

    Article  PubMed  Google Scholar 

  10. 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

    Article  PubMed  PubMed Central  Google Scholar 

  11. Carvalho AF, Heilig M, Perez A et al (2019) Alcohol use disorders. Lancet 394:781–792

    Article  PubMed  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. Brady KT, Randall CL (1999) Gender differences in substance use disorders. Psychiatr Clin North Am 22:241–252

    Article  CAS  PubMed  Google Scholar 

  15. Becker JB, Koob GF (2016) Sex differences in animal models: focus on addiction. Pharmacol Rev 68:242–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Larimer ME, Palmer RS, Marlatt GA (1999) Relapse prevention. An overview of Marlatt’s cognitive-behavioral model. Alcohol Res Health 23:151–160

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Anton RF (2000) Obsessive-compulsive aspects of craving: development of the obsessive compulsive drinking scale. Addiction 95(Suppl 2):S211–S217

    PubMed  Google Scholar 

  18. Sinha R (2009) Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict Biol 14:84–98

    Article  PubMed  Google Scholar 

  19. Tiffany ST, Conklin CA (2000) A cognitive processing model of alcohol craving and compulsive alcohol use. Addiction 95(Suppl 2):S145–S153

    Article  Google Scholar 

  20. Epstein DH, Kowalczyk WJ (2018) Compulsive seekers: our take. Two clinicians’ perspective on a new animal model of addiction. Neuropsychopharmacology 43:677–679

    Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. Everitt BJ, Robbins TW (2016) Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol 67:23–50

    Article  PubMed  Google Scholar 

  23. Hopf FW (2017) Do specific NMDA receptor subunits act as gateways for addictive behaviors? Genes Brain Behav 16:118–138

    Article  CAS  PubMed  Google Scholar 

  24. Hopf FW, Lesscher HM (2014) Rodent models for compulsive alcohol intake. Alcohol 48:253–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  26. Kranzler HR, Soyka M (2018) Diagnosis and pharmacotherapy of alcohol use disorder: a review. JAMA 320:815–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Spanagel R (2009) Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol Rev 89:649–705

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. Flores-Bonilla A, Richardson HN (2020) Sex differences in the neurobiology of alcohol use disorder. Alcohol Res 40:04

    PubMed  PubMed Central  Google Scholar 

  30. 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

    PubMed  PubMed Central  Google Scholar 

  31. Altemus M, Sarvaiya N, Neill Epperson C (2014) Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol 35:320–330

    Article  PubMed  PubMed Central  Google Scholar 

  32. Filkowski MM, Olsen RM, Duda B et al (2017) Sex differences in emotional perception: meta analysis of divergent activation. NeuroImage 147:925–933

    Article  PubMed  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Craig AD (2010) Once an island, now the focus of attention. Brain Struct Funct 214:395–396

    Article  CAS  PubMed  Google Scholar 

  37. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kolling N, Scholl J, Chekroud A et al (2018) Prospection, perseverance, and insight in sequential behavior. Neuron 99:1069–1082 e7

    Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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

    Article  CAS  PubMed  Google Scholar 

  42. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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

    Google Scholar 

  44. Chen NM, Lasek AM (2020) Perineuronal nets in the insula regulate aversion-resistant alcohol drinking. Addict Biol. 25:e12821

    Google Scholar 

  45. Arcurio LR, Finn PR, James TW (2015) Neural mechanisms of high-risk decisions-to-drink in alcohol-dependent women. Addict Biol 20:390–406

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. Claus ED, Ewing SW, Filbey FM et al (2011) Identifying neurobiological phenotypes associated with alcohol use disorder severity. Neuropsychopharmacology 36:2086–2096

    Article  PubMed  PubMed Central  Google Scholar 

  49. 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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  51. 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

    Article  PubMed  PubMed Central  Google Scholar 

  52. Lim AC, Cservenka A, Ray LA (2017) Effects of alcohol dependence severity on neural correlates of delay discounting. Alcohol Alcohol 52:506–515

    Article  PubMed  Google Scholar 

  53. 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

    Google Scholar 

  54. 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

    Article  PubMed  PubMed Central  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 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

    Google Scholar 

  58. McGuire JT, Botvinick MM (2010) Prefrontal cortex, cognitive control, and the registration of decision costs. Proc Natl Acad Sci USA 107:7922–7926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. 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

    Article  CAS  PubMed  Google Scholar 

  60. Hayden BY, Pearson JM, Platt ML (2011) Neuronal basis of sequential foraging decisions in a patchy environment. Nat Neurosci 14:933–939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Sterzer P, Kleinschmidt A (2010) Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 214:611–622

    Article  PubMed  Google Scholar 

  62. 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

    Google Scholar 

  63. Kolling N, Wittmann M, Rushworth MFS (2014) Multiple neural mechanisms of decision making and their competition under changing risk pressure. Neuron 81:1190–1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 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

    PubMed  PubMed Central  Google Scholar 

  69. Frankenstein UN, Richter W, McIntyre MC et al (2001) Distraction modulates anterior cingulate gyrus activations during the cold pressor test. NeuroImage 14:827–836

    Article  CAS  PubMed  Google Scholar 

  70. 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

    Article  PubMed  Google Scholar 

  71. Kaplan JT, Gimbel SI, Harris S (2016) Neural correlates of maintaining one’s political beliefs in the face of counterevidence. Sci Rep 6:39589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Aimone JA, Houser D, Weber B (2014) Neural signatures of betrayal aversion: an fMRI study of trust. Proc Biol Sci 281:20132127

    PubMed  PubMed Central  Google Scholar 

  73. Benoit RG, Gilbert SJ, Burgess PW (2011) A neural mechanism mediating the impact of episodic prospection on farsighted decisions. J Neurosci 31:6771–6779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 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

    Article  PubMed  PubMed Central  Google Scholar 

  75. Stoppel CM, Boehler CN, Strumpf H et al (2011) Neural processing of reward magnitude under varying attentional demands. Brain Res 1383:218–229

    Article  CAS  PubMed  Google Scholar 

  76. Grupe DW, Oathes DJ, Nitschke JB (2013) Dissecting the anticipation of aversion reveals dissociable neural networks. Cereb Cortex 23:1874–1883

    Article  PubMed  Google Scholar 

  77. Sadaghiani S, D’Esposito M (2015) Functional characterization of the Cingulo-Opercular network in the maintenance of tonic alertness. Cereb Cortex 25:2763–2773

    Article  PubMed  Google Scholar 

  78. 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

    Article  PubMed  Google Scholar 

  79. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. 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

  81. 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

  82. Ottenheimer D, Richard JM, Janak PH (2018) Ventral pallidum encodes relative reward value earlier and more robustly than nucleus accumbens. Nat Commun 9:4350

    Article  PubMed  PubMed Central  Google Scholar 

  83. Bari BA, Grossman CD, Lubin EE et al (2019) Stable representations of decision variables for flexible behavior. Neuron 103:922–933 e7

    Google Scholar 

  84. 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

    Google Scholar 

  85. Sadacca BF, Mukherjee N, Vladusich T et al (2016) The behavioral relevance of cortical neural ensemble responses emerges suddenly. J Neurosci 36:655–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Roebber JK, Izenwasser S, Chaudhari N (2015) Cocaine decreases saccharin preference without altering sweet taste sensitivity. Pharmacol Biochem Behav 133:18–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Moore JD, Kleinfeld D, Wang F (2014) How the brainstem controls orofacial behaviors comprised of rhythmic actions. Trends Neurosci 37:370–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Seif T, Simms JA, Lei K et al (2015) D-Serine and D-Cycloserine reduce compulsive alcohol intake in rats. Neuropsychopharmacology 40:2357–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 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

    Article  CAS  PubMed  Google Scholar 

  90. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. 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

    Article  PubMed  Google Scholar 

  92. 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

    Article  CAS  PubMed  Google Scholar 

  93. 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

    Article  CAS  PubMed  Google Scholar 

  94. Samson HH (2000) The microstructure of ethanol drinking: genetic and behavioral factors in the control of drinking patterns. Addiction 95(Suppl 2):S61–S72

    Article  PubMed  Google Scholar 

  95. 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

    Article  CAS  PubMed  Google Scholar 

  96. 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

    Google Scholar 

  97. Davis JD, Perez MC (1993) Food deprivation- and palatability-induced microstructural changes in ingestive behavior. Am J Phys 264:R97–R103

    CAS  Google Scholar 

  98. 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

    Article  PubMed  PubMed Central  Google Scholar 

  99. 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

    Article  CAS  PubMed  Google Scholar 

  100. 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

    Article  PubMed  Google Scholar 

  101. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. 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

    Article  PubMed  PubMed Central  Google Scholar 

  103. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. 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

    Article  PubMed  PubMed Central  Google Scholar 

  105. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. 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

    Article  PubMed  PubMed Central  Google Scholar 

  107. Patton MS, Heckman M, Kim C et al (2021) Compulsive alcohol consumption is regulated by dorsal striatum fast-spiking interneurons. Neuropsychopharmacology 46:351–359

    Article  CAS  PubMed  Google Scholar 

  108. Gutierrez R, Carmena JM, Nicolelis MA et al (2006) Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J Neurophysiol 95:119–133

    Article  PubMed  Google Scholar 

  109. Baird JP, Choe A, Loveland JL et al (2009) Orexin-a hyperphagia: hindbrain participation in consummatory feeding responses. Endocrinology 150:1202–1216

    Article  CAS  PubMed  Google Scholar 

  110. Voon V, Derbyshire K, Ruck C et al (2015) Disorders of compulsivity: a common bias towards learning habits. Mol Psychiatry 20:345–352

    Article  CAS  PubMed  Google Scholar 

  111. 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

    Article  PubMed  PubMed Central  Google Scholar 

  112. Han SW, Eaton HP, Marois R (2019) Functional fractionation of the Cingulo-Opercular network: alerting insula and updating cingulate. Cereb Cortex 29:2624–2638

    Article  PubMed  Google Scholar 

  113. Craig AD (2009) How do you feel – now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70

    Article  CAS  PubMed  Google Scholar 

  114. Jaramillo AA, Randall PA, Stewart S et al (2018b) Functional role for cortical-striatal circuitry in modulating alcohol self-administration. Neuropharmacology 130:42–53

    Article  CAS  PubMed  Google Scholar 

  115. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. 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

    Article  CAS  PubMed  Google Scholar 

  119. Whishaw IQ, Kolb B (1983) “Stick out your tongue”: tongue protrusion in neocortex and hypothalamic damaged rats. Physiol Behav 30:471–480

    Article  CAS  PubMed  Google Scholar 

  120. Castro AJ (1972) The effects of cortical ablations on tongue usage in the rat. Brain Res 45:251–253

    Article  CAS  PubMed  Google Scholar 

  121. Brimley CC, Mogenson GJ (1979) Oral motor deficits following lesions of the central nervous system in the rat. Am J Phys 237:R126–R131

    CAS  Google Scholar 

  122. 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

    Article  CAS  PubMed  Google Scholar 

  123. 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

    Article  PubMed  PubMed Central  Google Scholar 

  124. Horst NK, Laubach M (2009) The role of rat dorsomedial prefrontal cortex in spatial working memory. Neuroscience 164:444–456

    Article  CAS  PubMed  Google Scholar 

  125. 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

    Article  CAS  PubMed  Google Scholar 

  126. 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

    Article  Google Scholar 

  127. 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

    Article  PubMed  PubMed Central  Google Scholar 

  128. 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

    Article  PubMed  Google Scholar 

  129. Horst NK, Laubach M (2013) Reward-related activity in the medial prefrontal cortex is driven by consumption. Front Neurosci 7:56

    Article  PubMed  PubMed Central  Google Scholar 

  130. Stuss DT, Murphy KJ, Binns MA et al (2003) Staying on the job: the frontal lobes control individual performance variability. Brain 126:2363–2380

    Article  PubMed  Google Scholar 

  131. Stuss DT, Alexander MP, Shallice T et al (2005) Multiple frontal systems controlling response speed. Neuropsychologia 43:396–417

    Article  PubMed  Google Scholar 

  132. Croxson PL, Walton ME, O’Reilly JX et al (2009) Effort-based cost-benefit valuation and the human brain. J Neurosci 29:4531–4541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Rudebeck PH, Walton ME, Smyth AN et al (2006) Separate neural pathways process different decision costs. Nat Neurosci 9:1161–1168

    Article  CAS  PubMed  Google Scholar 

  135. Rich EL, Wallis JD (2016) Decoding subjective decisions from orbitofrontal cortex. Nat Neurosci 19:973–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Sharpe MJ, Killcross S (2015) The prelimbic cortex directs attention toward predictive cues during fear learning. Learn Mem 22:289–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Park J, Moghaddam B (2017) Impact of anxiety on prefrontal cortex encoding of cognitive flexibility. Neuroscience 345:193–202

    Article  CAS  PubMed  Google Scholar 

  138. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Uddin LQ, Nomi JS, Hebert-Seropian B et al (2017) Structure and function of the human insula. J Clin Neurophysiol 34:300–306

    Article  PubMed  PubMed Central  Google Scholar 

  140. 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

    Article  PubMed  Google Scholar 

  141. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. 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

    Article  PubMed  PubMed Central  Google Scholar 

  143. 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

    Article  CAS  PubMed  Google Scholar 

  144. Chua HF, Gonzalez R, Taylor SF et al (2009) Decision-related loss: regret and disappointment. NeuroImage 47:2031–2040

    Article  PubMed  Google Scholar 

  145. Burke CJ, Tobler PN (2011) Reward skewness coding in the insula independent of probability and loss. J Neurophysiol 106:2415–2422

    Article  PubMed  PubMed Central  Google Scholar 

  146. Kolling N, Behrens TE, Mars RB et al (2012) Neural mechanisms of foraging. Science 336:95–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Dosenbach NU, Visscher KM, Palmer ED et al (2006) A core system for the implementation of task sets. Neuron 50:799–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. 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

    Article  PubMed  PubMed Central  Google Scholar 

  149. 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

    Article  CAS  PubMed  Google Scholar 

  150. 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

    Article  CAS  PubMed  Google Scholar 

  151. 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

    Google Scholar 

  152. 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

    Google Scholar 

  153. 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

    Article  CAS  PubMed  Google Scholar 

  154. 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

    Article  PubMed  Google Scholar 

  155. Amarante LM, Caetano MS, Laubach M (2017) Medial frontal theta is entrained to rewarded actions. J Neurosci 37:10757–10769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. 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

    Article  CAS  PubMed  Google Scholar 

  157. Hollander JA, Lu Q, Cameron MD et al (2008) Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105:19480–19485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. 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

    Article  PubMed  PubMed Central  Google Scholar 

  159. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. 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

    Article  CAS  PubMed  Google Scholar 

  161. 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

    Article  CAS  PubMed  Google Scholar 

  162. 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

    Article  PubMed  Google Scholar 

  163. 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

    Article  PubMed  PubMed Central  Google Scholar 

  164. 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

    Article  PubMed  Google Scholar 

  165. 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

    Article  PubMed  PubMed Central  Google Scholar 

  166. 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

    Article  PubMed  Google Scholar 

  167. Kesner RP, Gilbert PE (2007) The role of the agranular insular cortex in anticipation of reward contrast. Neurobiol Learn Mem 88:82–86

    Article  PubMed  PubMed Central  Google Scholar 

  168. Smith KS, Graybiel AM (2013) A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron 79:361–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Stapleton JR, Lavine ML, Wolpert RL et al (2006) Rapid taste responses in the gustatory cortex during licking. J Neurosci 26:4126–4138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. 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

    Article  PubMed  PubMed Central  Google Scholar 

  173. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Mendez-Ruette M, Linsambarth S, Moraga-Amaro R et al (2019) The role of the rodent insula in anxiety. Front Physiol 10:330

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thatiane De Oliveira Sergio .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

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

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-3267-3_4

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-3266-6

  • Online ISBN: 978-1-0716-3267-3

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics