Circuits regulating pleasure and happiness: the evolution of reward-seeking and misery-fleeing behavioral mechanisms in vertebrates
- PMID: 26557051
- PMCID: PMC4615821
- DOI: 10.3389/fnins.2015.00394
Circuits regulating pleasure and happiness: the evolution of reward-seeking and misery-fleeing behavioral mechanisms in vertebrates
Abstract
The very first free-moving animals in the oceans over 540 million years ago must have been able to obtain food, territory, and shelter, as well as reproduce. Therefore, they would have needed regulatory mechanisms to induce movements enabling achievement of these prerequisites for survival. It can be useful to consider these mechanisms in primitive chordates, which represent our earliest ancestors, to develop hypotheses addressing how these essential parts of human behavior are regulated and relate to more sophisticated behavioral manifestations such as mood. An animal comparable to lampreys was the earliest known vertebrate with a modern forebrain consisting of old and new cortical parts. Lampreys have a separate dorsal pallium, the forerunner of the most recently developed part of the cerebral cortex. In addition, the lamprey extrapyramidal system (EPS), which regulates movement, is modern. However, in lampreys and their putative forerunners, the hagfishes, the striatum, which is the input part of this EPS, probably corresponds to the human centromedial amygdala, which in higher vertebrates is part of a system mediating fear and anxiety. Both animals have well-developed nuclear habenulae, which are involved in several critical behaviors; in lampreys this system regulates the reward system that reinforces appetitive-seeking behavior or the avoidance system that reinforces flight behavior resulting from negative inputs. Lampreys also have a distinct glutamatergic nucleus, the so-called habenula-projection globus pallidus, which receives input from glutamatergic and GABAergic signals and gives output to the lateral habenula. Via this route, this nucleus influences midbrain monoaminergic nuclei and regulates the food acquisition system. These various structures involved in motor regulation in the lampreys may be conserved in humans and include two complementary mechanisms for reward reinforcement and avoidance behaviors. The first system is associated with experiencing pleasure and the second with happiness. The activities of these mechanisms are regulated by a tract running via the habenula to the upper brainstem. Identifying the human correlate of the lamprey habenula-projecting globus pallidus may help in elucidating the mechanism of the antidepressant effects of glutamatergic drugs.
Keywords: addiction; amygdala; depression; evolution of CNS; habenula; ketamine; striatum.
Figures
![Figure 1](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0001.gif)
![Figure 2](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0002.gif)
![Figure 3](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0003.gif)
![Figure 4](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0004.gif)
![Figure 5](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0005.gif)
![Figure 6](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0006.gif)
![Figure 7](https://cdn.statically.io/img/www.ncbi.nlm.nih.gov/pmc/articles/instance/4615821/bin/fnins-09-00394-g0007.gif)
Similar articles
-
Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates.Front Neurosci. 2016 Nov 22;10:539. doi: 10.3389/fnins.2016.00539. eCollection 2016. Front Neurosci. 2016. PMID: 27920666 Free PMC article.
-
Evolution of circuits regulating pleasure and happiness with the habenula in control.CNS Spectr. 2019 Apr;24(2):233-238. doi: 10.1017/S1092852917000748. Epub 2017 Nov 1. CNS Spectr. 2019. PMID: 29091022
-
Circuits regulating pleasure and happiness: evolution and role in mental disorders.Acta Neuropsychiatr. 2018 Feb;30(1):29-42. doi: 10.1017/neu.2017.8. Epub 2017 May 5. Acta Neuropsychiatr. 2018. PMID: 28473012
-
The lamprey blueprint of the mammalian nervous system.Prog Brain Res. 2014;212:337-49. doi: 10.1016/B978-0-444-63488-7.00016-1. Prog Brain Res. 2014. PMID: 25194205 Review.
-
The blueprint of the vertebrate forebrain - With special reference to the habenulae.Semin Cell Dev Biol. 2018 Jun;78:103-106. doi: 10.1016/j.semcdb.2017.10.023. Epub 2017 Oct 26. Semin Cell Dev Biol. 2018. PMID: 29107476 Review.
Cited by
-
Non-human contributions to personality neuroscience: From fish through primates - a concluding editorial overview.Personal Neurosci. 2024 Feb 6;7:e5. doi: 10.1017/pen.2024.1. eCollection 2024. Personal Neurosci. 2024. PMID: 38384664 Free PMC article.
-
Habenular molecular targets for depression, impulsivity, and addiction.Expert Opin Ther Targets. 2023 Jul-Dec;27(9):757-761. doi: 10.1080/14728222.2023.2257390. Epub 2023 Sep 14. Expert Opin Ther Targets. 2023. PMID: 37705488 No abstract available.
-
Manipulating facial musculature with functional electrical stimulation as an intervention for major depressive disorder: a focused search of literature for a proposal.J Neuroeng Rehabil. 2023 May 16;20(1):64. doi: 10.1186/s12984-023-01187-8. J Neuroeng Rehabil. 2023. PMID: 37193985 Free PMC article. Review.
-
Neurosurgical Treatment of Pain.Brain Sci. 2022 Nov 20;12(11):1584. doi: 10.3390/brainsci12111584. Brain Sci. 2022. PMID: 36421909 Free PMC article. Review.
-
Non-human contributions to personality neuroscience - from fish through primates. An introduction to the special issue.Personal Neurosci. 2022 Sep 20;5:e11. doi: 10.1017/pen.2022.4. eCollection 2022. Personal Neurosci. 2022. PMID: 36258777 Free PMC article. Review.
References
-
- Carlson P. J., Diazgranados N., Nugent A. C., Ibrahim L., Luckenbaugh D. A., Brutsche N., et al. . (2013). Neural correlates of rapid antidepressant response to ketamine in treatment-resistant unipolar depression: a preliminary positron emission tomography study. Biol. Psychiatry 73, 1213–1221. 10.1016/j.biopsych.2013.02.008 - DOI - PMC - PubMed
LinkOut - more resources
Full Text Sources
Other Literature Sources