Skip to main content

Advertisement

SpringerLink
Log in

Food Reward-Induced Neurotransmitter Changes in Cognitive Brain Regions

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Recent evidence indicates that mechanisms involved in reward and mechanisms involved in learning interact, in that reward includes learning processes and learning includes reward processes. In spite of such interactions, reward and learning represent distinct functions. In the present study, as part of an examination of the differences in learning and reward mechanisms, it was assumed that food principally affects reward mechanisms. After a brief period of fasting, we assayed the release of three neurotransmitters and their associated metabolites in eight brain areas associated with learning and memory as a response to feeding. Using microdialysis for the assay, we found changes in the hippocampus, cortex, amygdala, and the thalamic nucleus, (considered cognitive areas), in addition to those in the nucleus accumbens and ventral tegmental area (considered reward areas). Extracellular dopamine levels increased in the nucleus accumbens, ventral tegmental area, amygdala, and thalamic nucleus, while they decreased in the hippocampus and prefrontal cortex. Dopamine metabolites increased in all areas tested (except the dorsal hippocampus); changes in norepinephrine varied with decreases in the accumbens, dorsal hippocampus, amygdala, and thalamic nucleus, and increases in the prefrontal cortex; serotonin levels decreased in all the areas tested; although its metabolite 5HIAA increased in two regions (the medial temporal cortex, and thalamic nucleus). Our assays indicate that in reward activities such as feeding, in addition to areas usually associated with reward such as the mesolimbic dopamine system, other areas associated with cognition also participate. Results also indicate that several transmitter systems play a part, with several neurotransmitters and several receptors involved in the response to food in a number of brain structures, and the changes in transmitter levels may be affected by metabolism and transport in addition to changes in release in a regionally heterogeneous manner. Food reward represents a complex pattern of changes in the brain that involve cognitive processes. Although food reward elements overlap with other reward systems sharing some neurotransmitter compounds, it significantly differs indicating a specific reward to process for food consumption. Like in other rewards, both learning and cognitive areas play a significant part in food reward.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Gambarana C, Masi F, Leggio B, Grappi S, Nanni G, Scheggi S, De Montis MG, Tagliamonte A (2003) Acquisition of a palatable-food-sustained appetitive behavior in satiated rats is dependent on the dopaminergic response to this food in limbic areas. Neuroscience 121:179–187

    Article  PubMed  CAS  Google Scholar 

  2. Bassareo V, Di Chiara G (1999) Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89:637–641

    Article  PubMed  CAS  Google Scholar 

  3. Roitman MF, Stuber GD, Phillips PE, Wightman RM, Carelli RM (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24:1265–1271

    Article  PubMed  CAS  Google Scholar 

  4. Di Chiara G (2005) Dopamine in disturbances of food and drug motivated behavior: a case of homology? Physiol Behav 86:9–10

    Article  PubMed  CAS  Google Scholar 

  5. Wise RA, Rompre PP (1989) Brain dopamine and reward. Annu Rev Psychol 40:191–225

    Article  PubMed  CAS  Google Scholar 

  6. Sziraki I, Sershen H, Benuck M, Hashim A, Lajtha A (1998) Receptor systems participating in nicotine-specific effects. Neurochem Int 33:445–457

    Article  PubMed  CAS  Google Scholar 

  7. Rossi S, Singer S, Shearman E, Sershen H, Lajtha A (2005) The effects of cholinergic and dopaminergic antagonists on nicotine-induced cerebral neurotransmitter changes. Neurochem Res 30:541–558

    Article  PubMed  CAS  Google Scholar 

  8. Sziraki I, Sershen H, Hashim A, Lajtha A (2002) Receptors in the ventral tegmental area mediating nicotine-induced dopamine release in the nucleus accumbens. Neurochem Res 27:253–261

    Article  PubMed  CAS  Google Scholar 

  9. Toth E, Vizi ES, Lajtha A (1993) Effect of nicotine on levels of extracellular amino acids in regions of the rat brain in vivo. Neuropharmacology 32:827–832

    Article  PubMed  CAS  Google Scholar 

  10. Shearman E, Rossi S, Szasz B, Juranyi Z, Fallon S, Pomara N, Sershen H, Lajtha A (2006) Changes in cerebral neurotransmitters and metabolites induced by acute donepezil and memantine administrations: a microdialysis study. Brain Res Bull 69:204–213

    Article  PubMed  CAS  Google Scholar 

  11. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates

  12. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598

    Article  PubMed  CAS  Google Scholar 

  13. Kelley AE, Schiltz CA, Landry CF (2005) Neural systems recruited by drug- and food-related cues: studies of gene activation in corticolimbic regions. Physiol Behav 86:11–14

    Article  PubMed  CAS  Google Scholar 

  14. Kelley AE (2004) Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44:161–179

    Article  PubMed  CAS  Google Scholar 

  15. Fuchs H, Nagel J, Hauber W (2005) Effects of physiological and pharmacological stimuli on dopamine release in the rat globus pallidus. Neurochem Int 47:474–481

    Article  PubMed  CAS  Google Scholar 

  16. Phillips AG, Ahn S, Floresco SB (2004) Magnitude of dopamine release in medial prefrontal cortex predicts accuracy of memory on a delayed response task. J Neurosci 24:547–553

    Article  PubMed  CAS  Google Scholar 

  17. Salamone JD, Correa M, Mingote S, Weber SM (2003) Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 305:1–8

    Article  PubMed  CAS  Google Scholar 

  18. Salamone JD, Correa M (2002) Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav Brain Res 137:3–25

    Article  PubMed  CAS  Google Scholar 

  19. Ikemoto S, Panksepp J (1996) Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav Neurosci 110:331–345

    Article  PubMed  CAS  Google Scholar 

  20. Cenci MA, Kalen P, Mandel RJ, Bjorklund A (1992) Regional differences in the regulation of dopamine and noradrenaline release in medial frontal cortex, nucleus accumbens and caudate-putamen: a microdialysis study in the rat. Brain Res 581:217–228

    Article  PubMed  CAS  Google Scholar 

  21. Nakazato T (2005) Striatal dopamine release in the rat during a cued lever-press task for food reward and the development of changes over time measured using high-speed voltammetry. Exp Brain Res 166:137–146

    Article  PubMed  CAS  Google Scholar 

  22. Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86:773–795

    Article  PubMed  CAS  Google Scholar 

  23. Cheng J, Feenstra MG (2006) Individual differences in dopamine efflux in nucleus accumbens shell and core during instrumental learning. Learn Mem 13:168–177

    Article  PubMed  CAS  Google Scholar 

  24. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494

    Article  PubMed  CAS  Google Scholar 

  25. Adinoff B (2004) Neurobiologic processes in drug reward and addiction. Harv Rev Psychiatry 12:305–320

    Article  PubMed  Google Scholar 

  26. Salamone JD (1994) The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav Brain Res 61:117–133

    Article  PubMed  CAS  Google Scholar 

  27. Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5:34–41

    Article  PubMed  CAS  Google Scholar 

  28. Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27:765–776

    Article  PubMed  Google Scholar 

  29. Will MJ, Franzblau EB, Kelley AE (2003) Nucleus accumbens mu-opioids regulate intake of a high-fat diet via activation of a distributed brain network. J Neurosci 23:2882–2888

    PubMed  CAS  Google Scholar 

  30. Reynolds SM, Berridge KC (2001) Fear and feeding in the nucleus accumbens shell: rostrocaudal segregation of GABA-elicited defensive behavior versus eating behavior. J Neurosci 21:3261–3270

    PubMed  CAS  Google Scholar 

  31. Seeman P, Wilson A, Gmeiner P, Kapur S (2006) Dopamine D2 and D3 receptors in human putamen, caudate nucleus, and globus pallidus. Synapse 60:205–211

    Article  PubMed  CAS  Google Scholar 

  32. Deadwyler SA, Hayashizaki S, Cheer J, Hampson RE (2004) Reward, memory and substance abuse: functional neuronal circuits in the nucleus accumbens. Neurosci Biobehav Rev 27:703–711

    Article  PubMed  Google Scholar 

  33. Avena NM, Rada P, Moise N, Hoebel BG (2006) Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 139:813–820

    Article  PubMed  CAS  Google Scholar 

  34. Fadel J, Sarter M, Bruno JP (2001) Basal forebrain glutamatergic modulation of cortical acetylcholine release. Synapse 39:201–212

    Article  PubMed  CAS  Google Scholar 

  35. Pratt WE, Kelley AE (2004) Nucleus accumbens acetylcholine regulates appetitive learning and motivation for food via activation of muscarinic receptors. Behav Neurosci 118:730–739

    Article  PubMed  CAS  Google Scholar 

  36. Hernadi L, Hiripi L, Dyakonova V, Gyori J, Vehovszky A (2004) Thee effect of food intake on the central monoaminergic system in the snail, Lymnaea stagnalis. Acta Biol Hung 55:185–194

    Article  PubMed  CAS  Google Scholar 

  37. Saul’skaia NB, Mikhailova MO (2001) [Th effect of D2-dopamine receptor blockade on glutamate release into extracellular space of Nucleus accumbens during food reinforcement]. Zh Vyssh Nerv Deiat Im I P Pavlova 51:254–255

    PubMed  CAS  Google Scholar 

  38. Westerink BH, Kwint HF, de Vries JB (1997) Eating-induced dopamine release from mesolimbic neurons is mediated by NMDA receptors in the ventral tegmental area: a dual-probe microdialysis study. J Neurochem 69:662–668

    Article  PubMed  CAS  Google Scholar 

  39. Cabeza DV, Carr KD (1998) Food restriction enhances the central rewarding effect of abused drugs. J Neurosci 18:7502–7510

    Google Scholar 

  40. Bassareo V, De Luca MA, Aresu M, Aste A, Ariu T, Di Chiara G (2003) Differential adaptive properties of accumbens shell dopamine responses to ethanol as a drug and as a motivational stimulus. Eur J Neurosci 17:1465–1472

    Article  PubMed  Google Scholar 

  41. Di Ciano P, Underwood RJ, Hagan JJ, Everitt BJ (2003) Attenuation of cue-controlled cocaine-seeking by a selective D3 dopamine receptor antagonist SB-277011-A. Neuropsychopharmacology 28:329–338

    Article  PubMed  CAS  Google Scholar 

  42. Bari AA, Pierce RC (2005) D1-like and D2 dopamine receptor antagonists administered into the shell subregion of the rat nucleus accumbens decrease cocaine, but not food, reinforcement. Neuroscience 135:959–968

    Article  PubMed  CAS  Google Scholar 

  43. Le Foll B, Goldberg SR, Sokoloff P (2005) The dopamine D3 receptor and drug dependence: effects on reward or beyond? Neuropharmacology 49:525–541

    Article  PubMed  CAS  Google Scholar 

  44. Paterson NE, Froestl W, Markou A (2005) Repeated administration of the GABAB receptor agonist CGP44532 decreased nicotine self-administration, and acute administration decreased cue-induced reinstatement of nicotine-seeking in rats. Neuropsychopharmacology 30:119–128

    Article  PubMed  CAS  Google Scholar 

  45. Markou A, Paterson NE, Semenova S (2004) Role of gamma-aminobutyric acid (GABA) and metabotropic glutamate receptors in nicotine reinforcement: potential pharmacotherapies for smoking cessation. Ann NY Acad Sci 1025:491–503

    Article  PubMed  CAS  Google Scholar 

  46. Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav.Brain Res 137:75–114

    Article  PubMed  CAS  Google Scholar 

  47. Jay TM (2003) Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 69:375–390

    Article  PubMed  CAS  Google Scholar 

  48. Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

Research described in this article was supported in part by Philip Morris USA Inc. and Philip Morris International.

Author information

Authors and Affiliations

  1. Nathan Kline Institute, Orangeburg, New York, 10962, USA

    Shaun Fallon, Erin Shearman, Henry Sershen & Abel Lajtha

Authors
  1. Shaun Fallon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erin Shearman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Henry Sershen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abel Lajtha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abel Lajtha.

Additional information

Special issue dedicated to Dr. Moussa Youdim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fallon, S., Shearman, E., Sershen, H. et al. Food Reward-Induced Neurotransmitter Changes in Cognitive Brain Regions. Neurochem Res 32, 1772–1782 (2007). https://doi.org/10.1007/s11064-007-9343-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-007-9343-8

Keywords

Search

Navigation