Afferent Projections to the Hypothalamus in Ranid Frogs

Neary, Timothy J.

doi:10.1159/000113254

Cited by 55 publications

(79 citation statements)

References 21 publications

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“…A projection from the LHb to the histaminergic tuberomammillary nucleus has also been demonstrated in rodents, but no direct projections to histaminergic neurons have been reported (58). In addition, anterogradely labeled fibers from the LHb have been shown to project to the hypothalamus in amphibians and mammals (58,59). This suggests that the LHb may have an as yet unappreciated role in regulating the histaminergic system, along with the dopaminergic and serotonergic systems.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Stephenson-Jones

Floros

Robertson

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

130

153

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The medial (MHb) and lateral (LHb) habenulae are a small group of nuclei that regulate the activity of monoaminergic neurons. Disruptions to these nuclei lead to deficits in a range of cognitive and motor functions from sleep to decision making. Interestingly, the habenular nuclei are present in all vertebrates, suggesting that they provide a common neural mechanism to influence these diverse functions. To unravel conserved habenula circuitry and approach an understanding of their basic function, we investigated the organization of these nuclei in the lamprey, one of the phylogenetically oldest vertebrates. Based on connectivity and molecular expression, we show that the MHb and LHb circuitry is conserved in the lamprey. As in mammals, separate populations of neurons in the LHb homolog project directly or indirectly to dopamine and serotonin neurons through a nucleus homologous to the GABAergic rostromedial mesopontine tegmental nucleus and directly to histamine neurons. The pallidal and hypothalamic inputs to the LHb homolog are also conserved. In contrast to other species, the habenula projecting pallidal nucleus is topographically distinct from the dorsal pallidum, the homolog of the globus pallidus interna. The efferents of the MHb homolog selectively target the interpeduncular nucleus. The MHb afferents arise from sensory (medial olfactory bulb, parapineal, and pretectum) and not limbic areas, as they do in mammals; consequently, the "context" in which this circuitry is recruited may have changed during evolution. Our results indicate that the habenular nuclei provide a common vertebrate circuitry to adapt behavior in response to rewards, stress, and other motivating factors.basal ganglia | neuromodulator T he habenular complex, a small group of nuclei in the epithalamus, links the limbic forebrain to mid-and hind-brain regions involved in adapting the internal cerebral state (1-4). Lesion and genetic inactivation studies have implicated the habenula in a range of functions from control of the circadian rhythm to adapting the behavioral response to fear and reward, as well as to higher cognitive functions, such as attention and value-based decision making (5-8). The habenula is present in all classes of vertebrates, including those that seemingly lack highlevel cognitive functions (9). This suggests that it regulates processes crucial to survival through a basic neural mechanism common to all vertebrates. To unravel the neural basis for the habenula's basic and complex functions, it will be important to elucidate the basic circuitry and determine how this has evolved to regulate higher cognitive functions.In mammals, the habenula is subdivided into two nuclei: the medial habenula (MHb) and lateral habenula (LHb) (10). The LHb receives value-related signals from the basal ganglia [globus pallidus interna/entopeduncular nucleus (GPi/EP)] as well as inputs from the diagonal band of Broca and the lateral hypothalamus (1, 11). The LHb projects to the GABAergic rostromedial mesopontine tegmental nucleus (RMTg), a...

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Section: Discussionmentioning

confidence: 99%

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Stephenson-Jones

Floros

Robertson

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

130

153

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“…This region also contains substance P and enkephalin fibers (Table 2) (Marin et al, 1998b) as well as a group of sexually dimorphic AVT neurons (González and Smeets, 1992;Moore et al, 2000), but only sparse neuropeptide Y immunoreactivity (Marin et al, 1998b). The amphibian BNST shares many similar hodological characteristics with the mammalian BNST, including reciprocal connections to the hypothalamus and HIP (Neary and Wilczynski, 1977;Allison and Wilczynski, 1991;Northcutt and Ronan, 1992;Neary, 1995).…”

Section: Amphibiansmentioning

confidence: 99%

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

O’Connell

Hofmann

2011

J of Comparative Neurology

859

879

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All animals evaluate the salience of external stimuli and integrate them with internal physiological information into adaptive behavior. Natural and sexual selection impinge on these processes, yet our understanding of behavioral decision-making mechanisms and their evolution is still very limited. Insights from mammals indicate that two neural circuits are of crucial importance in this context: the social behavior network and the mesolimbic reward system. Here we review evidence from neurochemical, tract-tracing, developmental, and functional lesion/stimulation studies that delineates homology relationships for most of the nodes of these two circuits across the five major vertebrate lineages: mammals, birds, reptiles, amphibians, and teleost fish. We provide for the first time a comprehensive comparative analysis of the two neural circuits and conclude that they were already present in early vertebrates. We also propose that these circuits form a larger social decision-making (SDM) network that regulates adaptive behavior. Our synthesis thus provides an important foundation for understanding the evolution of the neural mechanisms underlying reward processing and behavioral regulation. J. Comp. Neurol. 519:3599-3639, 2011. INDEXING TERMS: social behavior; comparative neuroanatomy; amphibian; reptile; bird; teleost; reward system; social behavior network; limbic system; neural circuitsThroughout their lives, all animals constantly face situations that provide either challenges (e.g., aggression, predation) or opportunities (e.g., reproduction, foraging, habitat selection) (for a detailed review, see O'Connell and Hofmann, 2011). In all cases, environmental cues are processed by sensory systems into a meaningful biological signal while internal physiological cues (e.g., condition, maturity) and prior experience are integrated at the same time. This process usually results in behavioral actions that are adaptive, i.e., beneficial to the animal. To accomplish this, an animal's nervous system must evaluate the salience of a stimulus and elicit a context-appropriate behavioral response. Despite tremendous progress in understanding the ecology and evolution of social behavior (Lorenz, 1952;Tinbergen, 1963;Lehrman, 1965;von Frisch, 1967;Krebs and Davies, 1993;Stephens, 2008), it is less understood where in the brain these decisions (e.g., about mate choice or territory defense) are made and how these brain circuits have arisen over the course of vertebrate evolution.Recent research has begun to decipher the neural basis of social decision-making. In mammals in particular, the neural circuits that evaluate stimulus salience and/or regulate social behavior have been uncovered to some degree: the mesolimbic reward system and social behavior network (Fig. 1). It is becoming increasingly clear that the reward system (including but not limited to the midbrain dopaminergic system) is the neural circuit where the salience of an external stimulus is evaluated (Deco and Rolls, 2005;Wickens et al., 2007), as appetitive beh...

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“…Northcutt, 1981], the origins of corticohypothalamic projections in frogs and geckos suggest otherwise. The dorsal pallium in anurans does not appear to have projections to the hypothalamus Alli son, 1989: Allison andWilczynski, 1991;Neary, 1995], yet the dorsal cortex in geckos has at least three subpopula tions with hypothalamic projections. Based on similarities in projections, we propose, instead, that the dorsal and medial cortices in reptiles, together, are homologous to the medial pallium anurans.…”

Section: Comparisons With Amphibians and Mammalsmentioning

confidence: 99%

“…Several hypothalamic projections from amygdalar, dorsal thalamic, and brainstem areas have been identified in frogs [Wilczynski and Allison, 1989;Allison and Wilczynski, 1991;Neary, 1995] and mammals [Swanson. 1987].…”

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confidence: 99%

Afferent Projections to the Lateral and Dorsomedial Hypothalamus in a Lizard, <i>Gekko gecko</i>

Bruce

Neary

1995

Brain Behav Evol

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Afferent projections to the lateral hypothalamic area and dorsomedial hypothalamic nucleus of the lizard Gekko gecko were studied after applications of wheat germ agglutinin conjugated to horseradish peroxidase. Large applications into the hypothalamus labeled several telencephalic populations not observed after smaller injections. These included the rostrolateral area of the dorsal cortex, a sheet of cells deep to the caudal pole of the lateral cortex, the external amygdala, and part of the dorsal ventricular ridge. Other populations were labeled in the diencephalon, including the supraoptic nucleus and nucleus ovalis; in the medulla the medial reticular area was labeled. Injections into the lateral hypothalamic area labeled neurons in the rostrolateral dorsal cortex, anterior, lateral, and dorsal septal nuclei, the striatoamygdalar area, nucleus accumbens, vertical limb of the diagonal band, nucleus of the accessory olfactory tract, the interstitial, ventral anterior, and ventral posterior amygdalar nuclei, several hypothalamic nuclei, and the posteroventral thalamic nucleus. Labeled brainstem populations included the ventral tegmental area, torus semicircularis, parvocellular and ventral isthmal nuclei, superior raphe, and the solitary nucleus. Injections in the dorsomedial hypothalamic nucleus labeled neurons in the rostral and caudolateral poles of the dorsal cortex, anterior septal nucleus, horizontal limb of the diagonal band, nucleus of the anterior commissure, several hypothalamic areas, the lateral habenula, the posteroventral thalamic nucleus, and cells scattered around the dorsolateral anterior thalamic nuclei. Labeled brainstem populations included the torus semicircularis, ventral tegmental area, superior raphe, parvocellular and ventral isthmal nuclei, and the lateral dorsal tegmental nucleus. The results of these studies are compared with findings in amphibians and mammals.

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Afferent Projections to the Hypothalamus in Ranid Frogs

Cited by 55 publications

References 21 publications

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

Afferent Projections to the Lateral and Dorsomedial Hypothalamus in a Lizard, <i>Gekko gecko</i>

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