journal article Jul 19, 2021

Chronic food restriction enhances dopamine-mediated intracranial self-stimulation

View at Publisher Save 10.1097/wnr.0000000000001700
Abstract
Dopamine-mediated reinforcement and behavioral adaptation is essential to survival. Here, we test the effects of food restriction on dopamine-mediated learning and reinforcement using optical intracranial self-stimulation (oICSS), an optogenetic version of conventional electrical ICSS (also known as brain stimulation reward, BSR). Using mouse genetic lines to express channelrhodopsin selectively in midbrain dopamine neurons, we demonstrate that genetically expressed channelrhodopsin can mediate optically evoked dopamine release and support self-stimulation in a lever-pressing paradigm. Using this midbrain dopamine oICSS preparation, we compare acquisition and rate of pressing in ad libitum versus food restricted mice. Food restriction facilitated both more rapid acquisition of self-stimulation behavior and higher rates of responding; reversing food status after acquisition modulated response vigor in already established behavior. These data suggest that food restriction enhances both the acquisition and expression of dopamine-reinforced self-stimulation responding. These data demonstrate the utility of oICSS for examining changes in reinforcement learning concomitant to neuroadaptations induced in dopamine signaling by experimental manipulations such as food restriction.
Topics

No keywords indexed for this article. Browse by subject →

References
27
[1]
Fulton "Appetite and reward." Front Neuroendocrinol (2010) 10.1016/j.yfrne.2009.10.003
[2]
Stouffer "Insulin enhances striatal dopamine release by activating cholinergic interneurons and thereby signals reward." Nat Commun (2015) 10.1038/ncomms9543
[3]
Carr "Chronic food restriction: enhancing effects on drug reward and striatal cell signaling." Physiol Behav (2007) 10.1016/j.physbeh.2006.09.021
[4]
Zhen "Chronic food restriction and dopamine transporter function in rat striatum." Brain Res (2006) 10.1016/j.brainres.2006.01.094
[5]
Pothos "Restricted eating with weight loss selectively decreases extracellular dopamine in the nucleus accumbens and alters dopamine response to amphetamine, morphine, and food intake." J Neurosci (1995) 10.1523/jneurosci.15-10-06640.1995
[6]
Haberny "Comparison of basal and D-1 dopamine receptor agonist-stimulated neuropeptide gene expression in caudate-putamen and nucleus accumbens of ad libitum fed and food-restricted rats." Brain Res Mol Brain Res (2005) 10.1016/j.molbrainres.2005.08.001
[7]
Ouyang "Food restriction induces synaptic incorporation of calcium-permeable AMPA receptors in nucleus accumbens." Eur J Neurosci (2017) 10.1111/ejn.13528
[8]
Lindblom "Increased mRNA levels of tyrosine hydroxylase and dopamine transporter in the VTA of male rats after chronic food restriction." Eur J Neurosci (2006) 10.1111/j.1460-9568.2005.04531.x
[9]
D’Cunha "Augmentation of heroin seeking following chronic food restriction in the Rat: differential role for dopamine transmission in the nucleus accumbens shell and core." Neuropsychopharmacology (2017) 10.1038/npp.2016.250
[10]
Carr "Homeostatic regulation of reward via synaptic insertion of calcium-permeable AMPA receptors in nucleus accumbens." Physiol Behav (2020) 10.1016/j.physbeh.2020.112850
[11]
Carrol "Increased drug-reinforced behavior due to food deprivation." Adv Behav Pharmacol (1984) 10.1016/b978-0-12-004704-8.50008-0
[12]
Shalev "Chronic food restriction augments the reinstatement of extinguished heroin-seeking behavior in rats." Addict Biol (2012) 10.1111/j.1369-1600.2010.00303.x
[13]
Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain.

James Olds, Peter Milner

Journal of Comparative and Physiological Psycholog... 1954 10.1037/h0058775
[14]
Carlezon "Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation." Nat Protoc (2007) 10.1038/nprot.2007.441
[15]
Cabeza de Vaca "Food restriction enhances the central rewarding effect of abused drugs." J Neurosci (1998) 10.1523/jneurosci.18-18-07502.1998
[16]
Abrahamsen "Curve-shift analysis of self-stimulation in food-restricted rats: relationship between daily meal, plasma corticosterone and reward sensitization." Brain Res (1995) 10.1016/0006-8993(95)00764-h
[17]
Elder "Effects of food deprivation and methamphetamine on fixed-ratio schedules of intracranial self-stimulation." Psychol Rep (1965) 10.2466/pr0.1965.16.3c.1225
[18]
Cabeza de Vaca "A progressive ratio schedule of self-stimulation testing in rats reveals profound augmentation of d-amphetamine reward by food restriction but no effect of a “sensitizing” regimen of d-amphetamine." Psychopharmacology (2004) 10.1007/s00213-003-1768-4
[19]
Optogenetics

Karl Deisseroth

Nature Methods 2011 10.1038/nmeth.f.324
[20]
Dopamine Neuron-Specific Optogenetic Stimulation in Rhesus Macaques

William R. Stauffer, Armin Lak, Aimei Yang et al.

Cell 2016 10.1016/j.cell.2016.08.024
[21]
Electrode calibration with a microfluidic flow cell for fast-scan cyclic voltammetry

Elly Sinkala, James E. McCutcheon, Matthew J. Schuck et al.

Lab on a Chip 2012 10.1039/c2lc40168a
[22]
Optogenetic investigation of neural circuits underlying brain disease in animal models

Kay M. Tye, Karl Deisseroth

Nature Reviews Neuroscience 2012 10.1038/nrn3171
[23]
Liu "Tissue specific expression of cre in rat tyrosine hydroxylase and dopamine active transporter-positive neurons." PLoS One (2016) 10.1371/journal.pone.0149379
[24]
Zhuang "Targeted gene expression in dopamine and serotonin neurons of the mouse brain." J Neurosci Methods (2005) 10.1016/j.jneumeth.2004.09.020
[25]
Cadoni "Selective psychostimulant sensitization by food restriction: differential changes in accumbens shell and core dopamine." Eur J Neurosci (2003) 10.1046/j.1460-9568.2003.02941.x
[26]
Zell "VTA Glutamate neuron activity drives positive reinforcement absent dopamine co-release." Neuron (2020) 10.1016/j.neuron.2020.06.011
[27]
Yoo "Ventral tegmental area glutamate neurons co-release GABA and promote positive reinforcement." Nat Commun (2016) 10.1038/ncomms13697
Cited By
4
Related

You May Also Like

Simultaneous EEG and fMRI of the alpha rhythm

Robin I. Goldman, Jerome Engel · 2002

971 citations

Why canʼt you tickle yourself?

Sarah-Jayne Blakemore, Daniel Wolpert · 2000

711 citations

Functional connectivity in a baseline resting-state network in autism

Vladimir L. Cherkassky, Rajesh K. Kana · 2006

520 citations