Neural and hormonal mechanisms of reproductive-related arousal in fishes

Forlano, Paul M.; Bass, Andrew H.

doi:10.1016/j.yhbeh.2010.10.006

Cited by 79 publications

(74 citation statements)

References 217 publications

(314 reference statements)

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“…The anterior tuberal nucleus is the putative teleostean homolog of the mammalian VMH (Forlano et al, 2005;Goodson, 2005;Forlano and Bass, 2011). It is located in the ventrocaudal part of the hypothalamus, contains sex steroid hormone receptors, and has a similar hodological profile (Folgueira et al, 2004a,b) in that it connects to the POA as well as several regions of the telencephalon.…”

Section: Teleostsmentioning

confidence: 99%

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

O’Connell

Hofmann

2011

J of Comparative Neurology

851

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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Section: Teleostsmentioning

confidence: 99%

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

O’Connell

Hofmann

2011

J of Comparative Neurology

851

879

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“…Homologous patterns of gene expression are considered to be any case where midshipman, mouse, and zebra finch each express FoxP2 in a comparable region in at least one study. The reader is referred to Forlano and Bass [2011] for a summary comparing forebrain regions in midshipman to those in tetrapods, but also see Wullimann [2009Wullimann [ , 2011, O'Connell and Hofmann [2011], Maximino et al [2013], and Biechl et al [2017] for teleosts in general; also see Mueller et al [2008] for comparisons to the striatum and the subpallium. For the midbrain PAG, see Goodson and Bass [2002] and Kittelberger and Bass [2013] for midshipman, and Kingsbury et al [2011] for birds.…”

Section: Comparisons With Birds and Mammalsmentioning

confidence: 99%

FoxP2 Expression in a Highly Vocal Teleost Fish with Comparisons to Tetrapods

Pengra

Marchaterre

Bass³

2018

Brain Behav Evol

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Motivated by studies of speech deficits in humans, several studies over the past two decades have investigated the potential role of a forkhead domain transcription factor, FoxP2, in the central control of acoustic signaling/vocalization among vertebrates. Comparative neuroanatomical studies that mainly include mammalian and avian species have mapped the distribution of FoxP2 expression in multiple brain regions that imply a greater functional significance beyond vocalization that might be shared broadly across vertebrate lineages. To date, reports for teleost fish have been limited in number and scope to nonvocal species. Here, we map the neuroanatomical distribution of FoxP2 mRNA expression in a highly vocal teleost, the plainfin midshipman (Porichthys notatus). We report an extensive overlap between FoxP2 expression and vocal, auditory, and steroid-signaling systems with robust expression at multiple sites in the telencephalon, the preoptic area, the diencephalon, and the midbrain. Label was far more restricted in the hindbrain though robust in one region of the reticular formation. A comparison with other teleosts and tetrapods suggests an evolutionarily conserved FoxP2 phenotype important to vocal-acoustic and, more broadly, sensorimotor function among vertebrates.

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“…The plainfin midshipman fish, Porichthys notatus, is a well-studied model system for understanding neural and hormonal mechanisms underlying vocal-acoustic communication in vertebrates (Bass and McKibben, 2003;Forlano and Bass, 2011), and thus is an ideal model to investigate structure-function of catecholamines in relation to well-delineated vocal and auditory circuits which may in turn provide important insights on the evolution of catecholamines in auditory-driven social behavior (Petersen et al, 2013). During the summer months in the intertidal zone off northern California and the Pacific Northwest, type I male midshipman excavate and defend nests under rocks, and court females at night by producing a long duration (>1 min) advertisement call via rapid contraction of the vocal musculature on the sides of the swimbladder (Bass and McKibben, 2003;Cohen and Winn, 1967).…”

Section: Introductionmentioning

confidence: 99%

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

Forlano

Kim

Krzyminska

et al. 2014

J of Comparative Neurology

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Although the neuroanatomical distribution of catecholaminergic (CA) neurons has been well documented across all vertebrate classes, few studies have examined CA connectivity to physiologically and anatomically identified neural circuitry that controls behavior. The goal of this study was to characterize CA distribution in the brain and inner ear of the plainfin midshipman fish (Porichthys notatus) with particular emphasis on their relationship with anatomically labeled circuitry that both produces and encodes social acoustic signals in this species. Neurobiotin labeling of the main auditory endorgan, the saccule, combined with tyrosine hydroxylase immunofluorescence (TH-ir) revealed a strong CA innervation of both the peripheral and central auditory system. Diencephalic TH-ir neurons in the periventricular posterior tuberculum, known to be dopaminergic, send ascending projections to the ventral telencephalon and prominent descending projections to vocal-acoustic integration sites, notably the hindbrain octavolateralis efferent nucleus, as well as onto the base of hair cells in the saccule via nerve VIII. Neurobiotin backfills of the vocal nerve in combination with TH-ir revealed CA terminals on all components of the vocal pattern generator which appears to largely originate from local TH-ir neurons but may include diencephalic projections as well. This study provides strong evidence for catecholamines

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Neural and hormonal mechanisms of reproductive-related arousal in fishes

Cited by 79 publications

References 217 publications

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

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

FoxP2 Expression in a Highly Vocal Teleost Fish with Comparisons to Tetrapods

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

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