Feeding and systemic d-amphetamine increase extracellular acetylcholine in the medial thalamus: A possible reward enabling function

doi:10.1016/j.neulet.2007.02.008

Neuroscience Letters

Volume 416, Issue 2, 12 April 2007, Pages 184-187

https://doi.org/10.1016/j.neulet.2007.02.008 Get rights and content

Abstract

Acetylcholine neurons that project forward from the midbrain are known to enable dopaminergic reward functions in the ventral tegmental area. The question is whether acetylcholine might also be released in the mediodorsal thalamus for the same general purposes. Rats with a microdialysis probe lodged in the mediodorsal thalamus were allowed to eat chow for 20 min after 16-h food deprivation or were given varying doses of d-amphetamine when fed ad libitum. The result in both cases was a significant increase in extracellular acetylcholine. During feeding, acetylcholine increased to 177% of baseline. In response to d-amphetamine (2.5 mg/kg), acetylcholine increased to 184%, and with a higher dose (5 mg/kg) to 400% of baseline. It is concluded that midbrain projections to limbic portions of the thalamus provide acetylcholine for behavioral activation. This cholinergic function theoretically plays a role in enabling the limbic circuits that pass through the thalamus for reinforcement of feeding and psychostimulant abuse.

Section snippets

Acknowledgements

Supported by NIMH grant MH-65024 to B. H. and CDCHT-ULA grant M-824-05-03-A to P. R.

References (32)

H.L. Alderson et al.
The effect of excitotoxic lesions of the pedunculopontine tegmental nucleus on performance of a progressive ratio schedule of reinforcement
Neuroscience
(2002)
H.L. Alderson et al.
An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioend rats
Neuroscience
(2004)
H.L. Alderson et al.
Involvement of the laterodorsal tegmental nucleus in the locomotor response to repeated nicotine administration
Neuroscience Lett.
(2005)
K.C. Berridge et al.
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Brain Res. Rev.
(1998)
R.F. Bolton et al.
Collateral axons of cholinergic pontine neurones projecting to midline, mediodorsal and parafascicular thalamic nuclei in the rat
J. Chem. Neuroanat.
(1993)
F. Chauveau et al.
Effects of ibotenic acid lesions of the mediodorsal thalamus on memory: relationship with emotional processes in mice
Behav. Brain Res.
(2005)
L. Churchill et al.
The mediodorsal nucleus of the thalamus in rats—II. Behavioral and neurochemical effects of GABA agonists
Neuroscience
(1996)
W.L. Inglis et al.
The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation
Prog. Neurobiol.
(1995)
T.A. Jenkins et al.
Determination of acetylcholine and dopamine content in thalamus and striatum after excitotoxic lesions of the pedunculopontine tegmental nucleus in rats
Neurosci Lett.
(2002)
M. Lepore et al.
N-methyl-D-aspartate lesions of the pedunculopontine nucleus block acquisition and impair maintenance of responding reinforced with brain stimulation
Neuroscience
(1996)

M.M. Mesulam et al.

Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1–Ch6)

Neuroscience

(1983)

M.F. Montaron et al.

Prefrontal cortex inputs of the nucleus accumbens-nigro-thalamic circuit

Neuroscience

(1996)

P.V. Rada et al.

Acetylcholine release in ventral tegmental area by hypothalamic self-stimulation, eating, and drinking

Pharmacol. Biochem. Behav.

(2000)

N.R. Swerdlow et al.

Lesions of the dorsomedial nucleus of the thalamus, medial prefrontal cortex and pedunculopontine nucleus: effects on locomotor activity mediated by nucleus accumbens-ventral pallidal circuitry

Brain Res.

(1987)

J.S. Yeomans et al.

Cholinergic involvement in lateral hypothalamic rewarding brain stimulation

Brain Res.

(1985)

J. Chen et al.

Roles of pedunculopontine tegmental cholinergic receptors in brain stimulation reward in the rat

Psychopharmacology

(2006)

Cited by (8)

Feeding behavior as seen through the prism of brain microdialysis
2011, Physiology and Behavior
Citation Excerpt :
Aversive stimulation of the LH releases Ach in the NAC but if the animal avoids LH stimulation (escape behavior), Ach decreases in the NAC [52]. Cholinergic inhibition in the NAc diminishes feeding behavior, but feeding enhances Ach release in the primary and non-primary motor areas of the frontal cortex [53], the dorsal hippocampus [54] and in the mediodorsal nucleus of the thalamus [55]. All of these areas contribute to the increased general locomotion in the first hours of the dark phase (the time of the cycle in which rats eat most of their meals) and enable the limbic circuits that pass through the thalamus to contribute to the reinforcement of feeding.
The knowledge of feeding behavior mechanisms gained through brain microdialysis is reviewed. Most of the chemical changes so far reported concern to the limbic system in rodents. A picture showing increases and decreases of extracellular neurotransmitters correlating to different aspects of feeding behavior is gradually emerging. Depending on the region, the same neurotransmitter may signal opposite aspects of feeding. Dopamine (DA) in the nucleus accumbens (NAC) correlates with food reward, stimulus saliency, and goal directed hyperlocomotion but in the ventromedial hypothalamus DA correlates with satiety and hypolocomotion. The findings accumulated in the last 25 years suggest that the control of a particular function relies on the interaction of several neurotransmitters rather than on a single neurotransmitter. The poor sensitivity of most analytical techniques hinders time and spatial resolution of microdialysis. Therefore, neurochemical correlates of short lasting behaviors are hard to figure out. As new and more sensitive analytical techniques are applied, new neurochemical correlates of feeding show up. Sometimes the proper analytical techniques are simply not available. As a consequence, critical signals such as neuropeptides are not yet completely placed in the puzzle. Despite such limitations, brain microdialysis has yielded a great deal of knowledge on the neurochemical basis of feeding.
Separable Substrates for Anticipatory and Consummatory Food Chemosensation
2008, Neuron
Citation Excerpt :
Since these stimuli were similarly pleasant and intense, our findings indicate that, within the context of conditioning, the amygdala encodes predictive meaning and/or biological relevance and not the perceived pleasantness of a cue. We also predicted similar responses in the OFC, midbrain, and ventral striatum, reflecting their involvement in taste anticipation, and in the mediodorsal (MD) thalamus, which represents an important olfactory nucleus involved in odor attention (Plailly et al., 2007) and which has recently been implicated in conditioning (Corbit et al., 2003; Li et al., 2004) and food reward (Rada et al., 2007; Small et al., 2005). Two experiments were performed.
Perception of the smell of a food precedes its ingestion and perception of its flavor. The neurobiological underpinnings of this association are not well understood. Of central interest is whether the same neural circuits code for anticipatory and consummatory phases. Here, we show that the amygdala and mediodorsal thalamus respond preferentially to food odors that predict immediate arrival of their associated drink (FO+) compared to food odors that predict delivery of a tasteless solution (FO−) and compared to the receipt of the drink. In contrast, the left insula/operculum responds preferentially to the drink, whereas the right insula/operculum and left orbitofrontal cortex respond to FO+ and drink. These findings indicate separable and overlapping representation of anticipatory and consummatory chemosensation. Moreover, since ratings of perceived pleasantness of FO+, FO−, and drink were similar, the response in the amygdala and thalamus cannot reflect acquired affective value but rather predictive meaning or biological relevance.
Blockade of mu-opioid receptors in the medial thalamus inhibits acquisition, but not expression, of morphine-induced conditioned place preference
2008, Neuroscience
Citation Excerpt :
Consistent with high density of mu-opioid receptors in the medial thalamus, microinjection of a mu-opioid receptor agonist into the MD produces a dose-related increase of dopamine release in the NAc (Klitenick and Kalivas, 1994). In addition, acetylcholine, which can play a role in behavioral reinforcement by facilitating dopamine release in the NAc, has also been found to increase in the medial thalamus in response to feeding and amphetamine (Rada et al., 2007). Given the anatomical and functional relationship between the medial thalamus and the NAc, it is very likely that the medial thalamus contributes to reinforcement and drug reward through modulation of dopamine levels in the NAc.
The medial thalamus contains abundant mu-opioid receptors and is activated by acute morphine administration. However, the role of the medial thalamus in the rewarding effects of morphine is unclear. The present study examined whether mu-opioid receptors of the medial thalamus influenced the acquisition and expression of morphine-induced conditioned place preference (CPP) in rats. An unbiased apparatus and biased subject assignment were used. Administration of morphine in increasing doses (2 mg/kg, 4 mg/kg, 6 mg/kg, 10 mg/kg, s.c.) was paired with an initially non-preferred chamber and saline administration was paired with an initially preferred chamber. Conditioning trials were conducted twice daily for 4 days. Microinjection of the irreversible mu-opioid receptor antagonist, β-funaltrexamine (5 μg/rat), into the medial thalamus 23 h prior to each morphine conditioning completely blocked the acquisition of CPP. However, microinjection of β-funaltrexamine into the medial thalamus after morphine conditioning trials, but 23 h prior to a test session, had no effect on the expression of CPP. It is concluded that mu-opioid receptors in the rat medial thalamus are involved in the acquisition, but not expression, of morphine-induced CPP.
Dopamine Supersensitivity: A Novel Hypothesis of Opioid-Induced Neurobiological Mechanisms Underlying Opioid-Stimulant Co-use and Opioid Relapse
2022, Frontiers in Psychiatry
The pharmacology of cocaine, amphetamines, and other stimulants
2014, The ASAM Principles of Addiction Medicine: Fifth Edition
Amphetamine stimulates movement through thalamocortical glutamate release
2014, Journal of Neurochemistry

View all citing articles on Scopus

View full text

Feeding and systemic d-amphetamine increase extracellular acetylcholine in the medial thalamus: A possible reward enabling function

Abstract

Section snippets

Acknowledgements

Neuroscience

Neuroscience

Neuroscience Lett.

Brain Res. Rev.

J. Chem. Neuroanat.

Behav. Brain Res.

Neuroscience

Prog. Neurobiol.

Neurosci Lett.

Neuroscience

Neuroscience

Neuroscience

Pharmacol. Biochem. Behav.

Brain Res.

Brain Res.

Roles of pedunculopontine tegmental cholinergic receptors in brain stimulation reward in the rat

Psychopharmacology