What are motivated behaviors?
The goal of this Research Topic was to assemble a diverse collection of current views of the hypothalamus relating to its role in the control of motivated behaviors. This editorial highlights the included articles directly and also indirectly via two perspectives (from George Fink and Menno Kruk) that frame the topic in a historical context. However, before these, it is apt to reconsider briefly what is meant by the term “motivated behaviors.”
According to the Oxford English Dictionary, the noun “motivation” (from adjective “motive”) stems from the Latin movēre, meaning “to move1,” and the noun “behavior” (from the verb “behave”) stems from a combination of “be-” (as a prefix) and “have,” conveying “to have or bear oneself (in a specified way),” that is to conduct oneself intentionally2. Motivated behaviors may then be thought of literally as the expression of intentional (or purposeful) movements. This understanding is reflected in their common description of being oriented, directed, or driven by a goal.
From a neuroscientific standpoint, the terms goal-oriented, goal-directed, and goal-driven, all convey essentially the same basic idea that orientation, direction, or drive toward a goal (that which motivates) occurs when a change in the internal (body) or external environment that is detected by the sensory division of the nervous system achieves a level of input stimulation that is sufficient to activate a behavioral output response from the body via the motor division of the nervous system. A goal is attained when the behavioral response counteracts the originating stimulus to a level at which it no longer stimulates the behavioral response (Figure 1). Examples include the drive to regulate body temperature, fluid balance, and energy status in response to sensed changes in these, in order to maintain homeostasis (Watts and Swanson, 2002).
Figure 1
Through a process of natural selection, animals have evolved motivated behaviors that support the life goals of survival and reproduction, and the motivated behaviors that fundamentally support these goals include those for which the hypothalamus plays a central role: ingestive (eating and drinking), agonistic (defensive and aggressive), sexual, and allied to these the control of behavioral state (the level of intrinsic behavioral arousal) (Swanson, 1987; Simerly, 2015).
In seeking to understand motivated behaviors, it is noteworthy that the distinction between movement per se and purposeful movement that is considered motivated behavior, is neither obvious nor absolute. For example, reflexes such as the patellar stretch reflex (knee-jerk) are not typically thought of as motivated behaviors, but they do involve movement that is ostensibly purposeful (postural retention in the case of the patellar reflex). Nevertheless, behaviors can to some extent be classified according to the parts of the nervous system that are necessary and sufficient for their expression.
Voluntary (cognitive) control of behavior requires the cerebral cortex; whereas control of innate (instinctive) behaviors is classically associated with the hypothalamus. At the lowest hierarchical level are reflex behaviors, such as the patellar reflex that involves a monosynaptic reflex arc between sensory and motor neurons in the spinal cord. Classic lesion experiments have shown that innate behaviors can be performed to some extent without the cerebral cortex, and spinal reflexes without the forebrain and much of the brainstem. However, it is also clear that hypothalamic (and lower) level behavioral control is to varying degrees subject to cerebral cortical control, and that all behavior occurs in concert with the activity of the body as a whole (Mogenson et al., 1980; Swanson and Mogenson, 1981; Swanson, 2000; Canteras, 2018).
Research Topic Contributions
Four of the included articles focus specifically on the spatially-extensive lateral hypothalamic area (LHA) that has received renewed attention in recent years, as successive inroads into its structural organization (Goto et al., 2005; Hahn, 2010; Hahn and Swanson, 2010, 2012, 2015; Canteras et al., 2011) have encouraged further forays into its functional roles (Leinninger, 2011; Li et al., 2011; Petrovich et al., 2012; Betley et al., 2013; Hsu et al., 2015). The first article, by Rangel et al., elucidates a novel role for an LHA region juxtaposed to the dorsomedial hypothalamic nucleus (the LHAjd), in relation to socially-relevant defensive behaviors; the second article, by Tyree and de Lecea, focuses on the relevance of LHA and ventral tegmental area (VTA) connections to the motor-output that is necessary for behavioral goal-seeking; the third article, by Petrovich, reviews recent evidence on the control of feeding behavior to support a view of the LHA as an interface between cognitive and sub-cognitive control; the fourth article, by Haller, delves into LHA involvement in aggression, and relates physiology to behavior, arguing the case that the LHA has a central role in deviant forms of aggressive behavior that are promoted by chronic glucocorticoid deficiency. In addition to these four LHA-related articles, a fifth, by Diniz and Bittencourt, relates broadly to them all as it provides a comprehensive and nicely illustrated review of the role of largely LHA-located melanin-concentrating hormone (MCH) neurons in relation to their participation in control of motivated behaviors.
Of the three remaining topic articles, one, by Hashikawa et al., also focuses on aggressive behavior: its neuroanatomical focus is the ventromedial hypothalamic nucleus (VMH), and a specific locus is the ventrolateral subdivision (VMHvl). Evidence to support a role for the VMHvl in generation of aggression is reviewed in relation to VMHvl neuronal connections. Hypothalamic connections are also the subject of an article by Micevych and Meisel, who focus their attention on circuit integration in relation to the control of female sexual behavior. Lastly, an article by Khan et al. demonstrates implementation of a novel computer-assisted method to facilitate interoperability between different brain atlases. To illustrate the approach (that has broad potential application), the authors use their hypothalamic datasets relating to behavioral control.
Historical Perspectives
To round out this editorial are two illustrated perspectives (edited by JDH). The first, by George Fink, is broadly relevant to the topic, and the second, by Menno Kruk, relates more closely to some of the included articles. Both are historically-informed vignettes that serve to frame the included articles and the topic, and are also offered to inspire future research into hypothalamic structure and function.
External Layer of the Median Eminence a Neurovascular Synapse
The external layer of the median eminence (MEex) is comprised of hypothalamic neuron axons that terminate on the primary plexus of hypophysial portal vessels, where they form neurovascular synapses (Figure 2). This organization has been exploited experimentally as a model system for investigating central neurotransmission (Fink and Smith, 1971), and to investigate interactions between multiple different neurotransmitters expressed by different types of hypothalamic neurons whose axons converge in the MEex. This is exemplified by physiological and pharmacological studies on the release into hypophysial portal blood of several neurohormones, most of which are neuropeptides, such as gonadotropin-releasing hormone (GnRH) and corticotropin releasing factor (CRF) (Fink, 2012). However, non-peptide neurotransmitters such as dopamine, which inhibits prolactin release, are also released into hypophysial portal blood. The hypophysial portal vessels (Figure 3) convey these neurohormones to the anterior pituitary gland where they stimulate or inhibit the release of pituitary hormones (Fink, 2012).
Figure 2
Figure 3
It is possible to collect hypophysial portal vessel blood experimentally and thereby determine directly the characteristics of neurohormone/transmitter release under experimental conditions. The interaction of neurohormones is exemplified by the potentiation of CRF anterior pituitary signaling by arginine vasopressin (AVP) (Gillies et al., 1982; Sheward and Fink, 1991). Portal vessel blood measurements may also provide information on the processing of neuropeptide precursors and identify potentially novel signaling molecules (Antoni et al., 1992; Fink et al., 1992; Caraty et al., 2010; Clarke et al., 2012).
Direct measurements of GnRH in hypophysial portal blood confirmed the existence of the estrogen-induced ovulatory surge in spontaneously ovulating mammals (Sarkar et al., 1976; Sherwood et al., 1980; Caraty et al., 2010; Clarke et al., 2012), and demonstrated the way that estrogen feedback moderates pulsatile GnRH release (Sarkar and Fink, 1980; Clarke and Cummins, 1982; Fink, 2018). The latter explains why pulsatile gonadotropin release occurs in ovariectomized, but not intact, rhesus monkeys (Dierschke et al., 1970), and the differences in gonadotropin pulse frequency in post-menopausal compared with pre-menopausal women (Yen et al., 1972). Similarly, glucocorticoid negative feedback inhibition of adrenocorticotropic hormone (ACTH) secretion from the anterior pituitary gland, depending on its duration, is mediated by central moderation of CRF and AVP release as well as well as blockade of the pituitary response to CRF (Plotsky et al., 1986; Fink et al., 1988; Sheward and Fink, 1991).
The post-synaptic consequences of MEex neurovascular synaptic signaling can readily be determined by studying pituitary hormone release, which has elucidated novel mechanisms such as the self-priming effect of GnRH, by which the decapeptide can increase by several fold its effect on gonadotropin release, can enable small pulses of GnRH to induce an ovulatory gonadotropin surge, and has been used extensively in artificial insemination, animal husbandry, and fish farming (Fink, 1995, 2015).
The Hypothalamic Ventromedial Nucleus: A Crucial Node in the Fight-Flight Balance?
Establishing that estrogen receptor-α (ESR1)-expressing neurons within the VMH ventrolateral part (VMHvl) are necessary and sufficient for aggressive behavior (Lin et al., 2011; Falkner et al., 2014; Kennedy et al., 2014) transformed the neuroscience of aggression, as it provided a specific locus from which to explore the “aggressive network” (Anderson, 2012; Yang et al., 2013, 2017; Hashikawa et al., 2016, 2017, 2018; Remedios et al., 2017; Hashikawa et al.). Other studies have identified cell groups in the amygdala and lateral septum that modify VMH activity (Choi et al., 2005; Wong et al., 2016). Moreover, activation of inhibitory (GABAergic) neurons in the medial amygdala can also elicit aggressive behavior (Hong et al., 2014). How the activity of these different cell groups is integrated is not fully understood, but a recent physiological experiment suggests a possible mechanism. Differential innervation of the “core” and “shell” of the VMH, directly from the basomedial amygdala, and indirectly from the anterior bed nucleus of the stria terminalis, produces “…a net inhibition or disinhibition of core neurons…depending on the firing rate of shell neurons,” imparting “…flexibility to this regulator of defensive and social behavior” (Yamamoto et al., 2018). Such flexibility might explain the episodic nature and context-sensitivity of fighting and underlie dynamic selection of appropriate behavioral responses in general (Brown et al., 1969b; Lammers et al., 1989; Haller et al., 1998a; Anderson, 2012; Yang et al., 2013, 2017; Hong et al., 2014; Kennedy et al., 2014; Hashikawa et al., 2016, 2018; Remedios et al., 2017; Todd et al., 2018; Todd and Machado, 2019).
Stimulation of the VMH and its surround is reported to evoke aggressive and defensive responses in several mammalian species (Yasukochi, 1960; Roberts et al., 1967; Brown et al., 1969a; Lipp and Hunsperger, 1978; Lammers et al., 1988; Kruk et al., 1983) (Figures 4, 5). However, predominant VHMvl association with overtly aggressive responses (Lin et al., 2011; Falkner et al., 2014, 2016; Kennedy et al., 2014) contrasts with VMH dorsolateral and central part association with defensive responses (Wang et al., 2015). This suggests the existence of a VMH-centric circuit for controlling opposing agonistic responses, echoing earlier ethological concepts of a mechanism for controlling “fight or flight” balance (Hinde, 1970).
Figure 4
Figure 5
In a manner similar to feedback (and feed-forward) control of the pituitary gland by circulating hormones (mentioned in the first perspective), the adrenocortical stress response (ACSR) (Joels et al., 2018) controls spontaneous and hypothalamus-elicited agonistic responses in experienced and inexperienced animals in different ways (Haller et al., 1998b, 2000a,b; Kruk et al., 1998, 2004, 2013; Mikics et al., 2007). An impaired ACSR tilts the balance toward “flight or freeze” in rats naïve to conflict but produces “pathological” attacks on opponents in bouts of spontaneous aggression (Haller et al., 2001, 2004). The behavioral changes correlate to altered hypothalamic excitability and enhanced amygdalar activity (Halasz et al., 2002; Kruk, 2014; Haller, 2018; Haller). A dynamic ACSR is clearly required for an adaptive response to social conflict. Interestingly, the absence of a well-timed ACSR in humans results in misguided aggression and poor conflict handling (Haller), possibly reflecting dysfunctional hypothalamic control.
Concluding Remarks
The ability to perform motivated behaviors (purposeful movements) is a defining characteristic of animals. In this ability, with respect to the control of fundamental behaviors in mammals and other vertebrates, the hypothalamus takes center stage. The works of twentieth century ethologists, exemplified in those of Tinbergen (1951), paved a path that has led inexorably into the hypothalamus, and they continue to inspire neuroscientists interested in the study of behavior.
The current Research Topic, and the articles that comprise it, reflect ongoing and growing interest in the hypothalamus, driven partly by the increasing availability of investigative tools borne of molecular biology and computer science. However, with regard to those tools, Tinbergen's advocacy for observations of nature, rather than availability of technique, to direct one's research, seems prescient. More generally, current interest is also driven by a renewed recognition that a better understanding of hypothalamus structure and function has potential relevance for numerous diseases that impact the vital and varied physiological and behavioral functions in which the hypothalamus plays a central role (Hahn et al., 2019).
Statements
Author contributions
JH wrote the editorial. GF and MK provided illustrated perspectives (edited by JH). All authors reviewed the editorial and provided editorial guidance.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Footnotes
1.^The Oxford English Dictionary Dictionary (OED). “motive, adj.”. Oxford University Press.
2.^The Oxford English Dictionary Dictionary (OED). “behave, v.”. Oxford University Press.
References
1
AndersonD. J. (2012). Optogenetics, sex, and violence in the brain: implications for psychiatry. Biol. Psychiatry71, 1081–1089. 10.1016/j.biopsych.2011.11.012
2
AntoniF. A.HunterE. F.LowryP. J.NobleJ. M.SecklJ. R. (1992). Atriopeptin: an endogenous corticotropin-release inhibiting hormone. Endocrinology130, 1753–1755. 10.1210/endo.130.3.1311248
3
BetleyJ. N.CaoZ. F.RitolaK. D.SternsonS. M. (2013). Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell155, 1337–1350. 10.1016/j.cell.2013.11.002
4
BrownJ. L.HunspergerR. W.RosvoldH. E. (1969a). Defence, attack, and flight elicited by electrical stimulation of the hypothalamus of the cat. Exp. Brain Res.8, 113–129. 10.1007/BF00234534
5
BrownJ. L.HunspergerR. W.RosvoldH. E. (1969b). Interaction of defence and flight reactions produced by simultaneous stimulation at two points in the hypothalamus of the cat. Exp. Brain Res.8, 130–149. 10.1007/BF00234535
6
CanterasN. S. (2018). Hypothalamic survival circuits related to social and predatory defenses and their interactions with metabolic control, reproductive behaviors and memory systems. Curr. Opin. Behav. Sci.24, 7–13. 10.1016/j.cobeha.2018.01.017
7
CanterasN. S.Ribeiro-BarbosaE. R.GotoM.Cipolla-NetoJ.SwansonL. W. (2011). The retinohypothalamic tract: comparison of axonal projection patterns from four major targets. Brain Res. Rev.65, 150–183. 10.1016/j.brainresrev.2010.09.006
8
CaratyA.FranceschiniI.HoffmanG. E. (2010). Kisspeptin and the preovulatory gonadotrophin-releasing hormone/luteinising hormone surge in the ewe: basic aspects and potential applications in the control of ovulation. J. Neuroendocrinol.22, 710–715. 10.1111/j.1365-2826.2010.02022.x
9
ChoiG. B.DongH. W.MurphyA. J.ValenzuelaD. M.YancopoulosG. D.SwansonL. W.et al. (2005). Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron46, 647–660. 10.1016/j.neuron.2005.04.011
10
ClarkeI. J.CampbellR.SmithJ. T.PrevotV.WrayS. (2012). Neuroendocrine control of reproduction, in Handbook of Neuroendocrinology, eds FinkG.PfaffD.LevineJ. (San Diego, CA: Academic Press/Elsevier), 197–235. 10.1016/B978-0-12-375097-6.10009-5
11
ClarkeI. J.CumminsJ. T. (1982). The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. Endocrinology111, 1737–1739. 10.1210/endo-111-5-1737
12
DierschkeD. J.BhattacharyaA. N.AtkinsonL. E.KnobilE. (1970). Circhoral oscillations of plasma LH levels in the ovariectomized rhesus monkey. Endocrinology87, 850–853. 10.1210/endo-87-5-850
13
FalknerA. L.DollarP.PeronaP.AndersonD. J.LinD. (2014). Decoding ventromedial hypothalamic neural activity during male mouse aggression. J. Neurosci.34, 5971–5984. 10.1523/JNEUROSCI.5109-13.2014
14
FalknerA. L.GrosenickL.DavidsonT. J.DeisserothK.LinD. (2016). Hypothalamic control of male aggression-seeking behavior. Nat. Neurosci.19, 596–604. 10.1038/nn.4264
15
FinkG. (1995). The self-priming effect of LHRH: a unique servomechanism and possible cellular model for memory. Front. Neuroendocrinol.16, 183–190. 10.1006/frne.1995.1006
16
FinkG. (2012). Neural control of the anterior lobe of the pituitary gland (Pars Distalis), in Handbook of Neuroendocrinology, eds FinkG.PfaffD. W.LevineJ. (San Diego, CA: Academic Press/Elsevier), 97–137. 10.1016/B978-0-12-375097-6.10005-8
17
FinkG. (2015). 60 YEARS OF NEUROENDOCRINOLOGY: MEMOIR: Harris' neuroendocrine revolution: of portal vessels and self-priming. J. Endocrinol.226, T13–24. 10.1530/JOE-15-0130
18
FinkG. (2018). Mathematical modeling of gonadotropin-releasing hormone signaling. Mol. Cell. Endocrinol.470, 34–35. 10.1016/j.mce.2017.09.034
19
FinkG.DowR. C.CasleyD.JohnstonC. I.BennieJ.CarrollS.et al. (1992). Atrial natriuretic peptide is involved in the ACTH response to stress and glucocorticoid negative feedback in the rat. J. Endocrinol.135, 37–43. 10.1677/joe.0.1350037
20
FinkG.RobinsonI. C.TannahillL. A. (1988). Effects of adrenalectomy and glucocorticoids on the peptides CRF-41, AVP and oxytocin in rat hypophysial portal blood. J. Physiol.401, 329–345. 10.1113/jphysiol.1988.sp017165
21
FinkG.SmithG. C. (1971). Ultrastructural features of the developing hypothalamo-hypophysial axis in the rat. A correlative study. Z. Zellforsch. Mikrosk. Anat.119, 208–226. 10.1007/BF00324522
22
GilliesG. E.LintonE. A.LowryP. J. (1982). Corticotropin releasing activity of the new CRF is potentiated several times by vasopressin. Nature299, 355–357. 10.1038/299355a0
23
GotoM.CanterasN. S.BurnsG.SwansonL. W. (2005). Projections from the subfornical region of the lateral hypothalamic area. J. Comp. Neurol.493, 412–438. 10.1002/cne.20764
24
HahnJ. D. (2010). Comparison of melanin-concentrating hormone and hypocretin/orexin peptide expression patterns in a current parceling scheme of the lateral hypothalamic zone. Neurosci.Lett.468, 12–17. 10.1016/j.neulet.2009.10.047
25
HahnJ. D.SpornsO.WattsA. G.SwansonL. W. (2019). Macroscale intrinsic network architecture of the hypothalamus. Proc. Natl. Acad. Sci. U.S.A.116, 8018–8027. 10.1073/pnas.1819448116
26
HahnJ. D.SwansonL. W. (2010). Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res. Rev.64, 14–103. 10.1016/j.brainresrev.2010.02.002
27
HahnJ. D.SwansonL. W. (2012). Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat. J. Comp Neurol.520, 1831–1890. 10.1002/cne.23064
28
HahnJ. D.SwansonL. W. (2015). Connections of the juxtaventromedial region of the lateral hypothalamic area in the male rat. Front. Syst. Neurosci.9:66. 10.3389/fnsys.2015.00066
29
HalaszJ.LipositsZ.KrukM. R.HallerJ. (2002). Neural background of glucocorticoid dysfunction-induced abnormal aggression in rats: involvement of fear- and stress-related structures. Eur. J. Neurosci.15, 561–569. 10.1046/j.0953-816x.2001.01883.x
30
HallerJ. (2018). The role of central and medial amygdala in normal and abnormal aggression: a review of classical approaches. Neurosci. Biobehav. Rev.85, 34–43. 10.1016/j.neubiorev.2017.09.017
31
HallerJ.AbrahamI.ZelenaD.JuhaszG.MakaraG. B.KrukM. R. (1998a). Aggressive experience affects the sensitivity of neurons towards pharmacological treatment in the hypothalamic attack area. Behav. Pharmacol.9, 469–475. 10.1097/00008877-199809000-00010
32
HallerJ.HalaszJ.MikicsE.KrukM. R. (2004). Chronic glucocorticoid deficiency-induced abnormal aggression, autonomic hypoarousal, and social deficit in rats. J. Neuroendocrinol.16, 550–557. 10.1111/j.1365-2826.2004.01201.x
33
HallerJ.HalaszJ.MikicsE.KrukM. R.MakaraG. B. (2000a). Ultradian corticosterone rhythm and the propensity to behave aggressively in male rats. J. Neuroendocrinol.12, 937–940. 10.1046/j.1365-2826.2000.00568.x
34
HallerJ.MillarS.KrukM. R. (1998b). Mineralocorticoid receptor blockade inhibits aggressive behaviour in male rats. Stress2, 201–207. 10.3109/10253899809167283
35
HallerJ.MillarS.Van De SchraafJ.De KloetR. E.KrukM. R. (2000b). The active phase-related increase in corticosterone and aggression are linked. J. Neuroendocrinol.12, 431–436. 10.1046/j.1365-2826.2000.00470.x
36
HallerJ.Van De SchraafJ.KrukM. R. (2001). Deviant forms of aggression in glucocorticoid hyporeactive rats: a model for 'pathological' aggression?J. Neuroendocrinol.13, 102–107. 10.1046/j.1365-2826.2001.00600.x
37
HashikawaK.HashikawaY.FalknerA.LinD. (2016). The neural circuits of mating and fighting in male mice. Curr. Opin. Neurobiol.38, 27–37. 10.1016/j.conb.2016.01.006
38
HashikawaK.HashikawaY.LischinskyJ.LinD. (2018). The neural mechanisms of sexually dimorphic aggressive behaviors. Trends Genet.34, 755–776. 10.1016/j.tig.2018.07.001
39
HashikawaK.HashikawaY.TremblayR.ZhangJ.FengJ. E.SabolA.et al. (2017). Esr1(+) cells in the ventromedial hypothalamus control female aggression. Nat. Neurosci.20, 1580–1590. 10.1038/nn.4644
40
HindeR. A. (1970). Animal Behavior, a synthesis of Ethology and Comparative Psychology International (Student Edition). London; Tokyo: McCraw Hill.
41
HongW.KimD. W.AndersonD. J. (2014). Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell158, 1348–1361. 10.1016/j.cell.2014.07.049
42
HsuT. M.HahnJ. D.KonanurV. R.NobleE. E.SuarezA. N.ThaiJ.et al. (2015). Hippocampus ghrelin signaling mediates appetite through lateral hypothalamic orexin pathways. Elife4:e11190. 10.7554/eLife.11190
43
JoelsM.KarstH.SarabdjitsinghR. A. (2018). The stressed brain of humans and rodents. Acta Physiol.223:e13066. 10.1111/apha.13066
44
KennedyA.AsahinaK.HoopferE.InagakiH.JungY.LeeH.et al. (2014). Internal states and behavioral decision-making: toward an integration of emotion and cognition. Cold Spring Harb. Symp. Quant. Biol.79, 199–210. 10.1101/sqb.2014.79.024984
45
KrukM. R. (2014). Hypothalamic attack: a wonderful artifact or a useful perspective on escalation and pathology in aggression? A viewpoint. Curr. Top. Behav. Neurosci.17, 143–188. 10.1007/7854_2014_313
46
KrukM. R.HalaszJ.MeelisW.HallerJ. (2004). Fast positive feedback between the adrenocortical stress response and a brain mechanism involved in aggressive behavior. Behav. Neurosci.118, 1062–1070. 10.1037/0735-7044.118.5.1062
47
KrukM. R.HallerJ.MeelisW.De KloetE. R. (2013). Mineralocorticoid receptor blockade during a rat's first violent encounter inhibits its subsequent propensity for violence. Behav. Neurosci.127, 505–514. 10.1037/a0033553
48
KrukM. R.Van Der PoelA. M.MeelisW.HermansJ.MostertP. G.MosJ.et al. (1983). Discriminant analysis of the localization of aggression-inducing electrode placements in the hypothalamus of male rats. Brain Res.260, 61–79. 10.1016/0006-8993(83)90764-3
49
KrukM. R.WestphalK. G.Van ErpA. M.Van AsperenJ.CaveB. J.SlaterE.et al. (1998). The hypothalamus: cross-roads of endocrine and behavioural regulation in grooming and aggression. Neurosci. Biobehav. Rev.23, 163–177. 10.1016/S0149-7634(98)00018-9
50
LammersJ. H.KrukM. R.MeelisW.Van Der PoelA. M. (1988). Hypothalamic substrates for brain stimulation-induced patterns of locomotion and escape jumps in the rat. Brain Res.449, 294–310. 10.1016/0006-8993(88)91045-1
51
LammersJ. H.Van DerN. J.KrukM. R.MeelisW.Van Der PoelG. M. (1989). Interactions between simultaneously activated behavioral systems in the rat. Behav. Neurosci.103, 784–789. 10.1037/0735-7044.103.4.784
52
LeinningerG. M. (2011). Lateral thinking about leptin: a review of leptin action via the lateral hypothalamus. Physiol. Behav.104, 572–581. 10.1016/j.physbeh.2011.04.060
53
LiF. W.DeurveilherS.SembaK. (2011). Behavioural and neuronal activation after microinjections of AMPA and NMDA into the perifornical lateral hypothalamus in rats. Behav. Brain Res.224, 376–386. 10.1016/j.bbr.2011.06.021
54
LinD.BoyleM. P.DollarP.LeeH.LeinE. S.PeronaP.et al. (2011). Functional identification of an aggression locus in the mouse hypothalamus. Nature470, 221–226. 10.1038/nature09736
55
LippH. P.HunspergerR. W. (1978). Threat, attack and flight elicited by electrical stimulation of the ventromedial hypothalamus of the marmoset monkey Callithrix jacchus. Brain Behav. Evol.15, 260–293. 10.1159/000123782
56
MikicsE.BarsyB.HallerJ. (2007). The effect glucocorticoids on aggressiveness in established colonies of rats. Psychoneuroendocrinology32, 160–170. 10.1016/j.psyneuen.2006.12.002
57
MogensonG. J.JonesD. L.YimC. Y. (1980). From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol.14, 69–97. 10.1016/0301-0082(80)90018-0
58
PetrovichG. D.HobinM. P.ReppucciC. J. (2012). Selective Fos induction in hypothalamic orexin/hypocretin, but not melanin-concentrating hormone neurons, by a learned food-cue that stimulates feeding in sated rats. Neuroscience224, 70–80. 10.1016/j.neuroscience.2012.08.036
59
PlotskyP. M.OttoS.SapolskyR. M. (1986). Inhibition of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation by delayed glucocorticoid feedback. Endocrinology119, 1126–1130. 10.1210/endo-119-3-1126
60
RemediosR.KennedyA.ZelikowskyM.GreweB. F.SchnitzerM. J.AndersonD. J. (2017). Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex. Nature550, 388–392. 10.1038/nature23885
61
RobertsW. W.SteinbergM. L.MeansL. W. (1967). Hypothalamic mechanisms for sexual, aggressive, and other motivational behaviors in the opossum, Didelphis virginiana. J. Comp. Physiol. Psychol.64, 1–15. 10.1037/h0024805
62
SarkarD. K.ChiappaS. A.FinkG.SherwoodN. M. (1976). Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature264, 461–463. 10.1038/264461a0
63
SarkarD. K.FinkG. (1980). Luteinizing hormone releasing factor in pituitary stalk plasma from long-term ovariectomized rats: effects of steroids. J. Endocrinol.86, 511–524. 10.1677/joe.0.0860511
64
SherwoodN. M.ChiappaS. A.SarkarD. K.FinkG. (1980). Gonadotropin-releasing hormone (GnRH) in pituitary stalk blood from proestrous rats: effects of anesthetics and relationship between stored and released GnRH and luteinizing hormone. Endocrinology107, 1410–1417. 10.1210/endo-107-5-1410
65
ShewardW. J.FinkG. (1991). Effects of corticosterone on the secretion of corticotrophin-releasing factor, arginine vasopressin and oxytocin into hypophysial portal blood in long-term hypophysectomized rats. J. Endocrinol.129, 91–98. 10.1677/joe.0.1290091
66
SimerlyR. B. (2015). Organization of the hypothalamus,: in The Rat Nervous System, 4th Edn. ed PaxinosG. (Amsterdam: Elsevier), 267–294. 10.1016/B978-0-12-374245-2.00013-9
67
SwansonL. W. (1987). The hypothalamus, in Handbook of Chemical Neuroanatomy, eds HökfeltT.BjörklundA.SwansonL. W. (Amsterdam: Elsevier), 1–124.
68
SwansonL. W. (2000). Cerebral hemisphere regulation of motivated behavior. Brain Res.886, 113–164. 10.1016/S0006-8993(00)02905-X
69
SwansonL. W.MogensonG. J. (1981). Neural mechanisms for the functional coupling of autonomic, endocrine and somatomotor responses in adaptive-behavior. Brain Res. Rev.3, 1–34. 10.1016/0165-0173(81)90010-2
70
TinbergenN. (1951). The Study of Instinct.Oxford: Oxford University Press.
71
ToddW. D.FenselauH.WangJ. L.ZhangR.MachadoN. L.VennerA.et al. (2018). A hypothalamic circuit for the circadian control of aggression. Nat. Neurosci.21, 717–724. 10.1038/s41593-018-0126-0
72
ToddW. D.MachadoN. L. (2019). A time to fight: circadian control of aggression and associated autonomic support. Auton. Neurosci.217, 35–40. 10.1016/j.autneu.2018.12.008
73
WangL.ChenI. Z.LinD. (2015). Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron85, 1344–1358. 10.1016/j.neuron.2014.12.025
74
WattsA. G.SwansonL. W. (2002). Anatomy of motivation, in Stevens' Handbook of Experimental Psychology, 3rd Edn. eds GallistelR.PashlerH. (New York, NY: John Wiley and Sons), 563–631. 10.1002/0471214426.pas0314
75
WongL. C.WangL.D'amourJ. A.YumitaT.ChenG.YamaguchiT.et al. (2016). Effective modulation of male aggression through lateral septum to medial hypothalamus projection. Curr. Biol.26, 593–604. 10.1016/j.cub.2015.12.065
76
YamamotoR.AhmedN.ItoT.GungorN. Z.PareD. (2018). Optogenetic study of anterior BNST and basomedial amygdala projections to the ventromedial hypothalamus. ENeuro5, 1–12. 10.1523/ENEURO.0204-18.2018
77
YangC. F.ChiangM. C.GrayD. C.PrabhakaranM.AlvaradoM.JunttiS. A.et al. (2013). Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell153, 896–909. 10.1016/j.cell.2013.04.017
78
YangT.YangC. F.ChizariM. D.MaheswaranathanN.BurkeK. J.Jr.BoriusM.et al. (2017). Social control of hypothalamus-mediated male aggression. Neuron95, 955–970 e954. 10.1016/j.neuron.2017.06.046
79
YasukochiG. (1960). Emotional responses elicited by electrical stimulation of the hypothalamus in cat. Folia Psychiatr. Neurol. Jpn.14, 260–267. 10.1111/j.1440-1819.1960.tb02246.x
80
YenS. S.TsaiC. C.NaftolinF.VandenbergG.AjaborL. (1972). Pulsatile patterns of gonadotropin release in subjects with and without ovarian function. J. Clin. Endocrinol. Metab.34, 671–675. 10.1210/jcem-34-4-671
Summary
Keywords
hypothalamus, brain, motivated behavior, innate behavior, sensory - motor coordination
Citation
Hahn JD, Fink G, Kruk MR and Stanley BG (2019) Editorial: Current Views of Hypothalamic Contributions to the Control of Motivated Behaviors. Front. Syst. Neurosci. 13:32. doi: 10.3389/fnsys.2019.00032
Received
29 March 2019
Accepted
08 July 2019
Published
13 August 2019
Volume
13 - 2019
Edited and reviewed by
Maria V. Sanchez-Vives, August Pi i Sunyer Biomedical Research Institute (IDIBAPS), Spain
Updates
Copyright
© 2019 Hahn, Fink, Kruk and Stanley.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Joel D. Hahn joelhahn@usc.edu
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.