The lamprey blueprint of the mammalian nervous system

2016

Front. Hum. Neurosci.

According to our model of the regulation of appetitive-searching vs. distress-avoiding behaviors, the motivation to display these essential conducts is regulated by two parallel cortico-striato-thalamo-cortical, re-entry circuits, including the core and the shell parts of the nucleus accumbens, respectively. An entire series of basal ganglia, running from the caudate nucleus on one side, to the centromedial amygdala on the other side, controls the intensity of these reward-seeking and misery-fleeing behaviors by stimulating the activity of the (pre)frontal and limbic cortices. Hyperactive motivation to display behavior that potentially results in reward induces feelings of hankering (relief leads to pleasure). Hyperactive motivation to exhibit behavior related to avoidance of misery results in dysphoria (relief leads to happiness). These two systems collaborate in a reciprocal fashion. In clinical depression, a mismatch exists between the activities of these two circuits: the balance is shifted to the misery-avoiding side. Five theories have been developed to explain the mechanism of depressive mood disorders, including the monoamine, biorhythm, neuro-endocrine, neuro-immune, and kindling/neuroplasticity theories. This paper describes these theories in relationship to the model (described above) of the regulation of reward-seeking vs. misery-avoiding behaviors. Chronic stress that leads to structural changes may induce the mismatch between the two systems. This mismatch leads to lack of pleasure, low energy, and indecisiveness, on one hand, and dysphoria, continuous worrying, and negative expectations on the other hand. The neuroplastic effects of monoamines, cortisol, and cytokines may mediate the induction of these structural alterations. Long-term exposure to stressful situations (particularly experienced during childhood) may lead to increased susceptibility for developing this condition. This hypothesis opens up the possibility of treating depression with psychotherapy. Genetic and other biological factors (toxic, infectious, or traumatic) may increase sensitivity to the induction of relevant neuroplastic changes. Reversal or compensation of these neuroplastic adjustments may explain the effects of biological therapies in treating depression.

Section: Description Of Our Modelmentioning

confidence: 99%

Section: Integration With Our Depression Modelmentioning

confidence: 99%

Section: Integration With Our Depression Modelmentioning

confidence: 99%

See 1 more Smart Citation

Circuits Regulating Pleasure and Happiness—Mechanisms of Depression

2016

Front. Hum. Neurosci.

“…The investigations made clear that the organization of the ancestral tetrapod (amphibian-like) amygdaloid complex is retained within more recent ancestors (Moreno and Gonzaléz, 2007). Evolution of the anamnio-amniotic (mammalian) “extrapyramidal” striatum probably occurred in a modular sense when a more lateral part of the striatum was added each time a neocortical area with a new function was added to the expanding neocortex (Grillner et al, 2013; Robertson et al, 2014). Probably in parallel to this neostriatum, the corresponding “extrapyramidal” globus pallidus and substantia nigra (reticulata and compacta) developed.…”

Section: Evolution Of Subcortical Structuresmentioning

confidence: 99%

Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates

2016

Front. Neurosci.

Appetitive-searching (reward-seeking) and distress-avoiding (misery-fleeing) behavior are essential for all free moving animals to stay alive and to have offspring. Therefore, even the oldest ocean-dwelling animal creatures, living about 560 million years ago and human ancestors, must have been capable of generating these behaviors. The current article describes the evolution of the forebrain with special reference to the development of the misery-fleeing system. Although, the earliest vertebrate ancestor already possessed a dorsal pallium, which corresponds to the human neocortex, the structure and function of the neocortex was acquired quite recently within the mammalian evolutionary line. Up to, and including, amphibians, the dorsal pallium can be considered to be an extension of the medial pallium, which later develops into the hippocampus. The ventral and lateral pallium largely go up into the corticoid part of the amygdala. The striatopallidum of these early vertebrates becomes extended amygdala, consisting of centromedial amygdala (striatum) connected with the bed nucleus of the stria terminalis (pallidum). This amygdaloid system gives output to hypothalamus and brainstem, but also a connection with the cerebral cortex exists, which in part was created after the development of the more recent cerebral neocortex. Apart from bidirectional connectivity with the hippocampal complex, this route can also be considered to be an output channel as the fornix connects the hippocampus with the medial septum, which is the most important input structure of the medial habenula. The medial habenula regulates the activity of midbrain structures adjusting the intensity of the misery-fleeing response. Within the bed nucleus of the stria terminalis the human homolog of the ancient lateral habenula-projecting globus pallidus may exist; this structure is important for the evaluation of efficacy of the reward-seeking response. The described organization offers a framework for the regulation of the stress response, including the medial habenula and the subgenual cingulate cortex, in which dysfunction may explain the major symptoms of mood and anxiety disorders.

“…4). Parallel to the expansion of the cerebral cortex, a subcortical extrapyramidal circuit evolved in a modular fashion (14,16). Every time a new function was acquired by a more developed ancestor of humans due to the expansion of the neocortex, a corresponding extrapyramidal circuit was created to support the execution of this function.…”

Section: Loonen and Ivanovamentioning

confidence: 99%

Circuits regulating pleasure and happiness: evolution and role in mental disorders

2017

Acta Neuropsychiatr.

Loonen AJM, Ivanova SA. Circuits regulating pleasure and happiness: evolution and role in mental disorders.Taking the evolutionary development of the forebrain as a starting point, the authors developed a biological framework for the subcortical regulation of human emotional behaviour which may offer an explanation for the pathogenesis of the principle symptoms of mental disorders. Appetitivesearching (reward-seeking) and distress-avoiding (misery-fleeing) behaviour are essential for all free-moving animals to stay alive and to have offspring. Even the oldest ocean-dwelling animal creatures, living about 560 million years ago and human ancestors, must therefore have been capable of generating these behaviours. Our earliest vertebrate ancestors, with a brain comparable with the modern lamprey, had a sophisticated extrapyramidal system generating and controlling all motions as well as a circuit including the habenula for the evaluation of the benefits of their actions. Almost the complete endbrain of the first land animals with a brain comparable with that of amphibians became assimilated into the human amygdaloid and hippocampal complex, whereas only a small part of the dorsal pallium and striatum developed into the ventral extrapyramidal circuits and the later insular cortex. The entire neocortex covering the hemispheres is of recent evolutionary origin, appearing first in early mammals. During the entire evolution of vertebrates, the habenular system was well conserved and maintained its function in regulating the intensity of reward-seeking (pleasurerelated) and misery-fleeing (happiness-related) behaviour. The authors propose that the same is true in humans. Symptomatology of human mental disorders can be considered to result from maladaptation within a similar amygdalo/ hippocampal-habenular-mesencephalic-ventral striatal system. Summations• The human laminated cerebral neocortex is of recent evolutionary origin and is not essential for the regulation of reward-seeking and misery-fleeing emotional behaviour.• Almost the entire telencephalon (endbrain) of human's earliest vertebrate ancestors became incorporated into our amygdaloid and hippocampal complexes.• The origin of many mental disorders can be found in the dysfunction of the amygdalo/hippocampalhabenular -upper brainstem circuitry.• Studying the modulation of neuronal circuit functioning in primitive vertebrates may offer suitable models by which to study the mechanism of human mental disorders, and to develop fundamentally different psychotropic treatments. Considerations• The reciprocal functional connectivity between specific cortical areas, for example, anterior cingulate, subgenual cingulate, orbitofrontal and ventromedial prefrontal cortices, and the various components of the subcortical regulatory neuronal system, remains to be determined.• It remains to be proven whether the connectivity of the corticoid amygdala through the extended amygdala and the hypothalamus regulates the lateral habenula, and that through the hippocampus and the septal ...