Exposure to cues associated with palatable food reward results in a dopamine D2 receptor-dependent suppression of evoked synaptic responses in the entorhinal cortex

Behavioral and Brain Functions

Volumn 9, Issue 1, 2013, Pages

  Hutter, Juliana A ^a   Chapman, C A ^a  

^a Concordia University ^*  (Canada)

Author keywords

Acetylcholine; Dopamine; Entorhinal cortex; Piriform cortex; Reward

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; DOPAMINE 2 RECEPTOR; ETICLOPRIDE; SCOPOLAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATION; CACAO; CONTROLLED STUDY; ELECTRIC POTENTIAL; ENTORHINAL CORTEX; EVOKED RESPONSE; FOOD REWARD; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; RECEPTOR BLOCKING; REWARD; SYNAPTIC POTENTIAL; WAKEFULNESS;

ANIMALS; BENZAZEPINES; CUES; DOPAMINE ANTAGONISTS; ENTORHINAL CORTEX; EVOKED POTENTIALS; MALE; OLFACTORY PATHWAYS; RATS; RATS, LONG-EVANS; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; REWARD; SALICYLAMIDES; SMELL;

EID: 84884919128     PISSN: None     EISSN: 17449081     Source Type: Journal    
DOI: 10.1186/1744-9081-9-37     Document Type: Article

References (55)

1. Burwell RD. The parahippocampal region: Corticocortical connectivity. Ann NY Acad Sci 2000, 911:25-42.
2. Lavenex P, Amaral DG. Hippocampal-neocortical interaction: A hierarchy of associativity. Hippocampus 2000, 10:420-430.
3. Squire LR, Stark CE, Clark RE. The medial temporal lobe. Annu Rev Neurosci 2004, 27:279-306.
4. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. Spatial representation in the entorhinal cortex. Science 2004, 305:1258-1264.
5. Caruana DA, Sorge RE, Stewart J, Chapman CA. Dopamine has bidirectional effects on synaptic responses to cortical inputs in layer II of the lateral entorhinal cortex. J Neurophysiol 2006, 96:3006-3015.
6. Bjorklund A, Lindvall O. Dopamine-containing systems in the CNS. Handbook of Chemical Neuroanatomy, volume 2 1984, 55-122. Amsterdam: Elsevier.
7. Loughlin SE, Fallon JH. Substantia nigra and ventral tegmental area projections to cortex: topography and collateralization. Neuroscience 1984, 11:425-435.
8. Oades RD, Halliday GM. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 1987, 434:117-165.
9. Akil M, Lewis DA. The distribution of tyrosine hydroxylase-immunoreactive fibers in the human entorhinal cortex. Neuroscience 1994, 60:857-874.
10. Erickson SL, Akil M, Levey AI, Lewis DA. Postnatal development of tyrosine hydroxylase- and dopamine transporter-immunoreactive axons in monkey rostral entorhinal cortex. Cereb Cortex 1998, 8:415-427.
11. Björklund A, Dunnett SB. Dopamine neuron systems in the brain: An update. TINS 2007, 30:194-202.
12. Rosenkranz JA, Johnston D. Dopaminergic regulation of neuronal excitability through modulation of I-h in layer V entorhinal cortex. J Neurosci 2006, 26:3229-3244.
13. Mayne EW, Craig MT, McBain CJ, Paulsen O. Dopamine suppresses persistent network activity via D1-like dopamine receptors in rat medial entorhinal cortex. Eur J Neurosci 2013, 37:1242-1247.
14. Pralong E, Jones RS. Interactions of dopamine with glutamate- and GABA-mediated synaptic transmission in the rat entorhinal cortex in vitro. Eur J Neurosci 1993, 5:760-767.
15. Stenkamp K, Heinemann U, Schmitz D. Dopamine suppresses stimulus-induced field potentials in layer III of rat medial entorhinal cortex. Neurosci Lett 1998, 255:119-121.
16. Caruana DA, Chapman CA. Dopaminergic suppression of synaptic transmission in the lateral entorhinal cortex. Neural Plast 2008, 2008:203514.
17. Goldman-Rakic PS, Muly EC, Williams GV. D1 receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 2000, 31:295-301.
18. Kroener S, Chandler LJ, Phillips PE, Seamans JK. Dopamine modulates persistent synaptic activity and enhances the signal-to-noise ratio in the prefrontal cortex. PLoS One 2009, 4:e6507.
19. Floresco SB, Blaha CD, Yang CR, Phillips AG. Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: cellular mechanisms of input selection. J Neurosci 2001, 21:2851-2860.
20. Dreher JC, Burnod Y. An integrative theory of the phasic and tonic modes of dopamine modulation in the prefrontal cortex. Neural Netw 2002, 15:583-602.
21. Arbuthnott GW, Wickens J. Space, time and dopamine. TINS 2007, 30:62-69.
22. Hasselmo ME. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 2006, 16:710-715.
23. Mitchell JB, Gratton A. Partial dopamine depletion of the prefrontal cortex leads to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli. J Neurosci 1992, 12:3609-3618.
24. Bassareo V, Di Chiara G. Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation to motivational state. Eur J Neurosci 1999, 11:4389-4397.
25. Richardson NR, Gratton A. Behavior-relevant changes in nucleus accumbens dopamine transmission elicited by food reinforcement: An electrochemical study in rat. J Neurosci 1996, 16:8160-8169.
26. Richardson NR, Gratton A. Changes in medial prefrontal cortical dopamine levels associated with response-contingent food reward: An electrochemical study in rat. J Neurosci 1998, 18:9130-9138.
27. Richardson NR, Gratton A. Changes in nucleus accumbens dopamine transmission associated with fixed- and variable-time schedule-induced feeding. Eur J Neurosci 2008, 27:2714-2723.
28. Gambarana C, Masi F, Leggio B, Grappi S, Nanni G, Scheggi S, De Montis MG, Tagliamonte A. Acquisition of a palatable-food-sustained appetitive behavior in satiated rats is dependent on the dopaminergic response to this food in limbic areas. Neuroscience 2003, 121:179-187.
29. Naleid AM, Grimms JW, Kessler DA, Sipols AJ, Aliakbari S, Bennett JL, Wells J, Fligewicz DP. Deconstructing the vanilla milkshake: The dominant effect of sucrose on self-administration of nutrient-flavour mixtures. Appetite 2008, 50:128-138.
30. Hernández L, Paredes D, Rada P. Feeding behavior as seen through the prism of brain microdialysis. Physiol Behav 2011, 104:47-56.
31. Merali Z, McIntosh J, Anisman H. Anticipatory cues differentially provoke in vivo peptidergic and monoaminergic release at the medial prefrontal cortex. Neuropsychopharmacology 2004, 29:1409-1418.
32. Schultz W. Multiple dopamine functions at different time courses. Annu Rev Neurosci 2007, 30:259-288.
33. Bassareo V, Musio P, Di Chiara G. Reciprocal responsiveness of nucleus accumbens shell and core dopamine to food- and drug-conditioned stimuli. Psychopharmacol (Berl) 2011, 214:687-697.
34. Wilson C, Nomikos GG, Collu M, Fibiger HC. Dopaminergic correlates of motivated behavior: Importance of drive. J Neurosci 1995, 15:5169-5178.
35. Keppel G. Design and Analysis: A Researcher's Handbook 1991, New Jersey: Prentice Hall, Upper Saddle River.
36. Klinkenberg I, Blokland A. The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev 2010, 34:1307-1350.
37. Hutter JA, Martel A, Trigiani L, Barrett SG, Chapman CA. Rewarding stimulation of the lateral hypothalamus induces a dopamine-dependent suppression of synaptic responses in the entorhinal cortex. Behav Brain Res 2013, 252:266-274.
38. Inglis FM, Day JC, Fibiger HC. Enhanced acetylcholine release in hippocampus and cortex during the anticipation and consumption of a palatable meal. Neurosci 1994, 62:1049-1056.
39. Pralong E, Magistretti PJ. Noradrenaline increases K-conductance and reduces glutamatergic transmission in the mouse entorhinal cortex by activation of alpha 2-adrenoreceptors. Eur J Neurosci 1995, 7:2370-2378.
40. Kitchigina V, Vankov A, Harley C, Sara SJ. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur J Neurosci 1997, 9:41-47.
41. Ma L, Shalinsky MH, Alonso A, Dickson CT. Effects of serotonin on intrinsic membrane properties of Layer II medial entorhinal cortex neurons. Hippocampus 2007, 17:114-129.
42. Richter M, Schilling T, Müller W. Muscarinic control of intracortical connections to layer II in rat entorhinal cortex slice. Neurosci Lett 1999, 273:200-202.
43. Cheong MY, Yun SH, Mook-Jung I, Joo I, Huh K, Jung MW. Cholinergic modulation of synaptic physiology in deep layer entorhinal cortex of the rat. J Neurosci Res 2001, 66:117-121.
44. Hamam BN, Sinai M, Poirier G, Chapman CA. Cholinergic suppression of excitatory synaptic responses in layer II of the medial entorhinal cortex. Hippocampus 2007, 17:103-113.
45. Sparks DW, Chapman CA. Cholinergic receptor activation induces a relative facilitation of synaptic responses in the entorhinal cortex during theta- and gamma-frequency stimulation of parasubicular inputs. Neuroscience 2013, 230:72-85.
46. Moser EI, Moser MB, Andersen P. Potentiation of dentate synapses initiated by exploratory learning in rats: Dissociation from brain temperature, motor activity, and arousal. Learn Mem 1994, 1:55-73.
47. Wu Y, Sutherland RJ. Hippocampal evoked potentials in novel environments: A behavioral clamping method. Behav Brain Res 2006, 172:63-71.
48. Grace AA, Floresco SB, Goto Y, Lodge DJ. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. TINS 2007, 30:220-227.
49. Bassareo V, De Luca MA, Di Chiara G. Differential expression of motivational stimulus properties by dopamine in nucleus accumbens shell versus core and prefrontal cortex. J Neurosci 2002, 22:4709-4719.
50. Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 2001, 124:1720-1733.
51. Rolls ET. Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol Behav 2005, 85:45-56.
52. McCabe C, Huber A, Harmer CJ, Cowen PJ. The D2 antagonist sulpiride modulates the neural processing of both rewarding and aversive stimuli in healthy volunteers. Psychopharmacol (Berl) 2011, 217:271-278.
53. Haase L, Green E, Murphy C. Males and females show differential brain activation to taste when hungry and sated in gustatory and reward areas. Appetite 2011, 57:421-434.
54. Caruana DA, Reed SJ, Sliz DJ, Chapman CA. Inhibiting dopamine reuptake blocks the induction of long-term potentiation and depression in the lateral entorhinal cortex of awake rats. Neurosci Lett 2007, 426:6-11.
55. Avena NM, Rada P, Hoebel BG. Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose. Neuroscience 2008, 156:865-871.