A brain motivated to play: insights into the neurobiology of playfulness

in Behaviour
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Play is an important part of normal childhood development and is seen in varied forms among many mammals. While not indispensable to normal development, playful social experiences as juveniles may provide an opportunity to develop flexible behavioural strategies when novel and uncertain situations arise as an adult. To understand the neurobiological mechanisms responsible for play and how the functions of play may relate to these neural substrates, the rat has become the model of choice. Play in the rat is easily quantified, tightly regulated, and can be modulated by genetic factors and postnatal experiences. Brain areas most likely to be involved in the modulation of play include regions within the prefrontal cortex, dorsal and ventral striatum, some regions of the amygdala, and habenula. This paper discusses what we currently know about the neurobiological substrates of play and how this can help illuminate functional questions about the putative benefits of play.

A brain motivated to play: insights into the neurobiology of playfulness

in Behaviour

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AchterbergE.J.M.TrezzaV.SiviyS.M.SchramaL.SchoffelmeerA.N.M.VanderschurenL.J.M.J. (2014). Amphetamine and cocaine suppress social play behavior in rats through distinct mechanisms. — Psychopharmacology 231: 1503-1515.

AchterbergE.J.M.van KerkhofL.W.M.DamsteegtR.TrezzaV.VanderschurenL.J.M.J. (2015). Methylphenidate and atomoxetine inhibit social play behavior through prefrontal and subcortical limbic mechanisms in rats. — J. Neurosci. 35: 161-169.

AchterbergE.J.M.van KerkhofL.W.M.ServadioM.van SwietenM.M.H.HouwingD.J.AalderinkM.DrielN.V.TrezzaV.VanderschurenL.J.M.J. (2016). Contrasting roles of dopamine and noradrenaline in the motivational properties of social play behavior in rats. — Neuropsychopharmacology 41: 858-868.

AguilarR.CaramesJ.M.EspinetA. (2009). Effects of neonatal handling on playfulness by means of reversal of the desire to play in rats (Rattus norvegicus). — J. Comp. Psychol. 123: 347-356.

ArnstenA.F.T.SteereJ.C.HuntR.D. (1996). The contribution of α2-noradrenergic mechanisms to prefrontal cortical cognitive function: potential significance for attention-deficit hyperactivity disorder. — Arch. Gen. Psychol. 53: 448-455.

ArnstenA.F.T.SteereJ.C.JentschD.J.LiB.M. (1998). Noradrenergic influences on prefrontal cortical cognitive function: opposing actions at postjunctional α1 versus α2-adrenergic receptors. — Adv. Pharmacol. 42: 764-766.

BaarendseP.J.J.CounotteD.S.O’DonnellP.VanderschurenL.J.M.J. (2013). Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function. — Neuropsychopharmacology 38: 1485-1494.

BeattyW.W.CostelloK.B.BerryS.L. (1984). Suppression of play fighting by amphetamine: effects of catecholamine antagonists, agonists and synthesis inhibitors. — Pharmacol. Biochem. Behav. 20: 747-755.

BeattyW.W.DodgeA.M.DodgeL.J.WhiteK.PankseppJ. (1982). Psychomotor stimulants, social deprivation and play in juvenile rats. — Pharmacol. Biochem. Behav. 16: 417-422.

BellH.C.McCaffreyD.R.ForgieM.L.KolbB.PellisS.M. (2009). The role of the medial prefrontal cortex in the play fighting of rats. — Behav. Neurosci. 123: 1158-1168.

BellH.C.PellisS.M.KolbB. (2010). Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices. — Behav. Brain Res. 207: 7-13.

BerridgeK.C. (2007). The debate over dopamine’s role in reward: the case for incentive salience. — Psychopharmacology 191: 391-431.

BiancoI.H.WilsonS.W. (2009). The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. — Phil. Trans. Roy Soc. B: Biol. Sci. 364: 1005-1020.

BoufleurN.AntoniazziC.T.D.PaseC.S.BenvegnúD.M.DiasV.T.SegatH.J.RoversiK.RoversiK.NoraM.D.KoakoskiaG.RosaJ.G.BarcellosL.J.G.BürgerM.E. (2013). Neonatal handling prevents anxiety-like symptoms in rats exposed to chronic mild stress: behavioral and oxidative parameters. — Stress 16: 321-330.

BrownH.D.BakerP.M.RagozzinoM.E. (2010). The parafascicular thalamic nucleus concomitantly influences behavioral flexibility and dorsomedial striatal acetylcholine output in rats. — J. Neurosci. 30: 14390-14398.

BrunelliS.A.NieR.WhippleC.WinigerV.HoferM.A.ZimmerbergB. (2006). The effects of selective breeding for infant ultrasonic vocalizations on play behavior in juvenile rats. — Physiol. Behav. 87: 527-536.

BurgdorfJ.PankseppJ. (2001). Tickling induces reward in adolescent rats. — Physiol. Behav. 72: 167-173.

BurgdorfJ.KroesR.A.MoskalJ.R.PfausJ.G.BrudzynskiS.M.PankseppJ. (2008). Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. — J. Comp. Psychol. 122: 357-367.

BurghardtG.M. (2005). The genesis of animal play: testing the limits. — MIT PressCambridge, MA.

CalcagnettiD.J.SchechterM.D. (1992). Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. — Physiol. Behav. 51: 667-672.

CaldjiC.TannenbaumB.SharmaS.FrancisD.PlotskyP.M.MeaneyM.J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. — Proc. Natl. Acad. Sci. USA 95: 5335-5340.

CardinalR.N.ParkinsonJ.A.HallJ.EverittB.J. (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. — Neurosci. Biobehav. Rev. 26: 321-352.

CesaroP.Nguyen-LegrosJ.PollinB.LaplanteS. (1985). Single intralaminar thalamic neurons project to cerebral cortex, striatum and nucleus reticularis thalami. A retrograde anatomical tracing study in the rat. — Brain Res. 325: 29-37.

DaenenE.W.P.M.WolterinkG.GerritsM.A.F.M.Van ReeJ.M. (2002). The effects of neonatal lesions in the amygdala or ventral hippocampus on social behaviour later in life. — Behav. Brain Res. 136: 571-582.

DragunowM.FaullR. (1989). The use of c-fos as a metabolic marker in neuronal pathway tracing. — J. Neurosci. Methods 29: 261-265.

FergusonS.A.CadaA.M. (2004). Spatial learning/memory and social and nonsocial behaviors in the spontaneously hypertensive, Wistar–Kyoto and Sprague–Dawley rat strains. — Pharmacol. Biochem. Behav. 77: 583-594.

FieldE.F.PellisS.M. (1994). Differential effects of amphetamine on the attack and defense components of play fighting in rats. — Physiol. Behav. 56: 325-330.

GordonN.S.Kollack-WalkerS.AkilH.PankseppJ. (2002). Expression of c-fos gene activation during rough and tumble play in juvenile rats. — Brain Res. Bull. 57: 651-659.

GrahamK.L. (2011). Coevolutionary relationship between striatum size and social play in nonhuman primates. — Am. J. Primatol. 73: 314-322.

HimmlerB.T.KiskoT.M.EustonD.R.KolbB.PellisS.M. (2014). Are 50-kHz calls used as play signals in the playful interactions of rats? I. Evidence from the timing and context of their use. — Behav. Proc. 106: 60-66.

HimmlerB.T.PellisS.M.KolbB. (2013). Juvenile play experience primes neurons in the medial prefrontal cortex to be more responsive to later experiences. — Neurosci. Lett. 556: 42-45.

HumphreysA.P.EinonD.R. (1981). Play as a reinforcer for maze-learning in juvenile rats. — Anim. Behav. 29: 259-270.

HumphriesM.D.PrescottT.J. (2010). The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. — Prog. Neurobiol. 90: 385-417.

IkemotoS.PankseppJ. (1999). The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. — Brain Res. Rev. 31: 6-41.

KamitakaharaH.MonfilsM.H.ForgieM.L.KolbB.PellisS.M. (2007). The modulation of play fighting in rats: role of the motor cortex. — Behav. Neurosci. 121: 164-176.

KiskoT.M.EustonD.R.PellisS.M. (2015a). Are 50-kHz calls used as play signals in the playful interactions of rats? III. The effects of devocalization on play with unfamiliar partners as juveniles and as adults. — Behav. Proc. 113: 113-121.

KiskoT.M.HimmlerB.T.HimmlerS.M.EustonD.R.PellisS.M. (2015b). Are 50-kHz calls used as play signals in the playful interactions of rats? II. Evidence from the effects of devocalization. — Behav. Proc. 111: 25-33.

KnutsonB.BurgdorfJ.PankseppJ. (1998). Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. — J. Comp. Psychol. 112: 65-73.

KnutsonB.BurgdorfJ.PankseppJ. (2002). Ultrasonic vocalizations as indices of affective states in rats. — Psychol. Bull. 128: 961-977.

LeccaS.MeyeF.J.MameliM. (2014). The lateral habenula in addiction and depression: an anatomical, synaptic and behavioral overview. — Eur. J. Neurosci. 39: 1170-1178.

LecourtierL.KellyP.H. (2007). A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. — Neurosci. Biobehav. Rev. 31: 658-672.

LewisK.P.BartonR.A. (2006). Amygdala size and hypothalamus size predict social play frequency in nonhuman primates: a comparative analysis using independent contrasts. — J. Comp. Psychol. 120: 31-37.

LiuD.DiorioJ.TannenbaumB.CaldjiC.FrancisD.FreemanA.SharmaS.PearsonD.PlotskyP.M.MeaneyM.J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. — Science 277: 1659-1662.

MacLeanP.D. (1985). Brain evolution relating to family, play, and the separation call. — Arch. Gen. Psychol. 42: 405-417.

MacLeanP.D. (1990). The triune brain in evolution: role in paleocerebral functions. — PlenumNew York, NY.

MadrugaC.XavierL.L.AchavalM.SanvittoG.L.LucionA.B. (2006). Early handling, but not maternal separation, decreases emotional responses in two paradigms of fear without changes in mesolimbic dopamine. — Behav. Brain Res. 166: 241-246.

ManducaA.CampolongoP.PalmeryM.VanderschurenL.J.M.J.CuomoV.TrezzaV. (2014). Social play behavior, ultrasonic vocalizations and their modulation by morphine and amphetamine in Wistar and Sprague–Dawley rats. — Psychopharmacology 231: 1661-1673.

MeaneyM.J.DodgeA.M.BeattyW.W. (1981). Sex-dependent effects of amygdaloid lesions on the social play of prepubertal ras. — Physiol. Behav. 26: 467-472.

MeerloP.HorvathK.M.NagyG.M.BohusB.KoolhaasJ.M. (1999). The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. — J. Neuroendocrinol. 11: 925-933.

MenardJ.L.ChampagneD.L.MeaneyM.J. (2004). Variations of maternal care differentially influence ‘fear’ reactivity and regional patterns of cFos immunoreactivity in response to the shock-probe burying test. — Neuroscience 129: 297-308.

MooreC.L.PowerK.L. (1992). Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring. — Dev. Psychobiol. 25: 165-182.

MurphyM.R.MacLeanP.D.HamiltonS.C. (1981). Species-typical behavior of hamsters deprived from birth of the neocortex. — Science 213: 459-461.

NakamuraY.OtakeK.TokunoH. (2006). The parafascicular nucleus relays spinal inputs to the striatum: an electron microscope study in the rat. — Neurosci. Res. 56: 73-79.

NiesinkR.J.M.Van ReeJ.M. (1989). Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. — Neuropharmacology 28: 411-418.

NormansellL.PankseppJ. (1990). Effects of morphine and naloxone on play-rewarded spatial discrimination in juvenile rats. — Dev. Psychobiol. 23: 75-83.

PankseppJ. (1981). The ontogeny of play in rats. — Dev. Psychobiol. 14: 327-332.

PankseppJ.BeattyW.W. (1980). Social deprivation and play in rats. — Behav. Neural Biol. 30: 197-206.

PankseppJ.BishopP. (1981). An autoradiographic map of [3H]diprenorphine binding in rat brain: effects of social interaction. — Brain Res. Bull. 7: 405-410.

PankseppJ.SiviyS.M.NormansellL. (1984). The psychobiology of play: theoretical and methodological considerations. — Neurosci. Biobehav. Rev. 8: 465-492.

PankseppJ.JalowiecJ.DeEskinaziF.G.BishopP. (1985). Opiates and play dominance in juvenile rats. — Behav. Neurosci. 99: 441-453.

PankseppJ.NormansellL.CoxJ.F.SiviyS.M. (1994). Effects of neonatal decortication on the social play of juvenile rats. — Physiol. Behav. 56: 429-443.

PankseppJ.BurgdorfJ.TurnerC.GordonN. (2003). Modeling ADHD-type arousal with unilateral frontal cortex damage in rats and beneficial effects of play therapy. — Brain Cogn. 52: 97-105.

ParentC.I.MeaneyM.J. (2008). The influence of natural variations in maternal care on play fighting in the rat. — Dev. Psychobiol. 50: 767-776.

PaulM.J.TerranovaJ.I.ProbstC.K.MurrayE.K.IsmailN.I.de VriesG.J. (2014). Sexually dimorphic role for vasopressin in the development of social play. — Front. Behav. Neurosci. 8: 58.

PellisS.M.PellisV.C. (1990). Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. — Dev. Psychobiol. 23: 215-231.

PellisS.M.PellisV.C. (1991). Attack and defense during play fighting appear to be motivationally independent behaviors in muroid rodents. — Psych. Rec. 41: 175-184.

PellisS.M.PellisV.C. (2009). The playful brain: venturing to the limits of neuroscience. — OneworldOxford.

PellisS.M.PellisV.C.WhishawI.Q. (1992). The role of the cortex in play fighting by rats: developmental and evolutionary implications. — Brain Behav. Evol. 39: 270-284.

PellisS.M.CastenedaE.McKennaM.M.Tran-NguyenL.T.WhishawI.Q. (1993a). The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats. — Neurosci. Lett. 158: 13-15.

PellisS.M.PellisV.C.McKennaM.M. (1993b). Some subordinates are more equal than others: play fighting amongst adult subordinate male rats. — Aggr. Behav. 19: 385-393.

PellisS.M.FieldE.F.SmithL.K.PellisV.C. (1997). Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. — Neurosci. Biobehav. Rev. 21: 105-120.

PellisS.M.HastingsE.ShimizuT.KamitakaharaH.KomorowskaJ.ForgieM.L.KolbB. (2006). The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and nonplayful social contexts. — Behav. Neurosci. 120: 72-84.

RagozzinoM.E. (2007). The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. — Ann. NY Acad. Sci. 1121: 355-375.

RainekiC.LucionA.B.WeinbergJ. (2014). Neonatal handling: an overview of the positive and negative effects. — Dev. Psychobiol. 56: 1613-1625.

ReinhartC.J.PellisS.M.McIntyreD.C. (2004). Development of play fighting in kindling-prone (FAST) and kindling-resistant (SLOW) rats: how does the retention of phenotypic juvenility affect the complexity of play?Dev. Psychobiol. 45: 83-92.

ReinhartC.J.McIntyreD.C.MetzG.A.PellisS.M. (2006). Play fighting between kindling-prone (FAST) and kindling-resistant (SLOW) rats. — J. Comp. Psychol. 120: 19-30.

RobbinsT.W.ArnstenA.F.T. (2009). The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. — Annu. Rev. Neurosci. 32: 267-287.

RobinsonD.L.ZitzmanD.L.SmithK.J.SpearL.P. (2011). Fast dopamine release events in the nucleus accumbens of early adolescent rats. — Neuroscience 176: 296-307.

SefferD.SchwartingR.K.W.WöhrM. (2014). Pro-social ultrasonic communication in rats: insights from playback studies. — J. Neurosci. Methods 234: 73-81.

SiviyS.M.HarrisonK.A. (2008). Effects of neonatal handling on play behavior and fear towards a predator odor in juvenile rats (Rattus norvegicus). — J. Comp. Psychol. 122: 1-8.

SiviyS.M.PankseppJ. (1985). Dorsomedial diencephalic involvement in the juvenile play of rats. — Behav. Neurosci. 99: 1103-1113.

SiviyS.M.PankseppJ. (1987a). Juvenile play in the rat: thalamic and brain stem involvement. — Physiol. Behav. 41: 103-114.

SiviyS.M.PankseppJ. (1987b). Sensory modulation of juvenile play in rats. — Dev. Psychobiol. 20: 39-55.

SiviyS.M.PankseppJ. (2011). In search of the neurobiological substrates for social playfulness in mammalian brains. — Neurosci. Biobehav. Rev. 35: 1821-1830.

SiviyS.M.BalikoC.N.BowersK.S. (1997). Rough-and-tumble play behavior in Fischer-344 and Buffalo rats: effects of social isolation. — Physiol. Behav. 61: 597-602.

SiviyS.M.LoveN.J.DeCiccoB.M.GiordanoS.B.SeifertT.L. (2003). The relative playfulness of juvenile Lewis and Fischer-344 rats. — Physiol. Behav. 80: 385-394.

SiviyS.M.CrawfordC.A.AkopianG.WalshJ.P. (2011). Dysfunctional play and dopamine physiology in the Fischer 344 rat. — Behav. Brain Res. 220: 294-304.

SmithK.S.GraybielA.M. (2013). Using optogenetics to study habits. — Brain Res. 1511: 102-114.

SmithL.K.FieldE.F.ForgieM.L.PellisS.M. (1996). Dominance and age-related changes in the play fighting of intact and post-weaning castrated male rats (Rattus norvegicus). — Aggr. Behav. 22: 215-226.

SpinkaM.NewberryR.C.BekoffM. (2001). Mammalian play: training for the unexpected. — Q. Rev. Biol. 76: 141-168.

SutherlandR.J. (1982). The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. — Neurosci. Biobehav. Rev. 6: 1-13.

TrezzaV.VanderschurenL.J.M.J. (2008). Cannabinoid and opioid modulation of social play behavior in adolescent rats: differential behavioral mechanisms. — Eur. Neuropsychopharmacol. 18: 519-530.

TrezzaV.DamsteegtR.VanderschurenL.J.M.J. (2009). Conditioned place preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. — Eur. Neuropsychopharmacol. 19: 659-669.

TrezzaV.BaarendseP.J.J.VanderschurenL.J.M.J. (2010). The pleasures of play: pharmacological insights into social reward mechanisms. — Trends Pharmacol. Sci. 31: 463-469.

TrezzaV.CampolongoP.VanderschurenL.J.M.J. (2011a). Evaluating the rewarding nature of social interactions in laboratory animals. — Dev. Cog. Neurosci. 1: 444-458.

TrezzaV.DamsteegtR.AchterbergE.J.M.VanderschurenL.J.M.J. (2011b). Nucleus accumbens μ-opioid receptors mediate social reward. — J. Neurosci. 31: 6362-6370.

TrezzaV.DamsteegtR.ManducaA.PetrosinoS.Van KerkhofL.W.M.PasterkampR.J.VanderschurenL.J.M.J. (2012). Endocannabinoids in amygdala and nucleus accumbens mediate social play reward in adolescent rats. — J. Neurosci. 32: 14899-14908.

Van den BergC.L.HolT.Van ReeJ.M.SpruijtB.M.EvertsH.KoolhaasJ.M. (1999). Play is indispensable for an adequate development of coping with social challenges in the rat. — Dev. Psychobiol. 34: 129-138.

van HasseltF.N.TieskensJ.M.TrezzaV.KrugersH.J.VanderschurenL.J.M.J.JoëlsM. (2012). Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. — Physiol. Behav. 106: 701-706.

van KerkhofL.W.M. (2013). The brain at play: neural substrates of social play behaviour in adolescent rats. — PhD thesis University of Utrecht Utrecht.

van KerkhofL.W.M.DamsteegtR.TrezzaV.VoornP.VanderschurenL.J.M.J. (2013a). Functional integrity of the habenula is necessary for social play behaviour in rats. — Eur. J. Neurosci. 38: 3465-3475.

van KerkhofL.W.M.DamsteegtR.TrezzaV.VoornP.VanderschurenL.J.M.J. (2013b). Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum. — Neuropsychopharmacology 38: 1899-1909.

van KerkhofL.W.M.TrezzaV.MulderT.GaoP.VoornP.VanderschurenL.J.M.J. (2014). Cellular activation in limbic brain systems during social play behaviour in rats. — Brain Struct. Funct. 219: 1181-1211.

VanderschurenL.J.M.J.TrezzaV. (2014). What the laboratory rat has taught us about social play behavior: role in behavioral development and neural mechanisms. — Curr. Topics Behav. Neurosci. 16: 189-212.

VanderschurenL.J.M.J.NiesinkR.J.M.SpruijtB.M.Van ReeJ.M. (1995a). μ- and κ-opioid receptor-mediated opioid effects on social play in juvenile rats. — Eur. J. Pharmacol. 276: 257-266.

VanderschurenL.J.M.J.NiesinkR.J.M.SpruijtB.M.Van ReeJ.M. (1995b). Effects of morphine on different aspects of social play in juvenile rats. — Psychopharmacology 117: 225-231.

VanderschurenL.J.M.J.SteinE.A.WiegantV.M.Van ReeJ.M. (1995c). Social play alters regional brain opioid receptor binding in juvenile rats. — Brain Res. 680: 148-156.

VanderschurenL.J.M.J.SpruijtB.M.HolT.NiesinkR.J.M.Van ReeJ.M. (1996). Sequential analysis of social play behavior in juvenile rats: effects of morphine. — Behav. Brain Res. 72: 89-95.

VanderschurenL.J.M.J.NiesinkR.J.M.Van ReeJ.M. (1997). The neurobiology of social play behavior in rats. — Neurosci. Biobehav. Rev. 21: 3090-3326.

VanderschurenL.J.M.J.TrezzaV.Griffioen-RooseS.SchiepersO.J.G.Van LeeuwenN.De VriesT.J.SchoffelmeerA.N.M. (2008). Methylphenidate disrupts social play behavior in adolescent rats. — Neuropsychopharmacology 33: 2946-2956.

VeenemaA.H.BredewoldR.De VriesG.J. (2013). Sex-specific modulation of juvenile social play by vasopressin. — Psychoneuroendocrinology 38: 2554-2561.

Von FrijtagJ.C.SchotM.van den BosR.SpruijtB.M. (2002). Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. — Dev. Psychobiol. 41: 58-69.

VoornP.VanderschurenL.J.M.J.GroenewegenH.J.RobbinsT.W.PennartzC.M.A. (2004). Putting a spin on the dorsal-ventral divide of the striatum. — Trends Neurosci. 27: 468-474.

WebberE.S.HarmonK.M.BeckwithT.J.PeñaS.BurgdorfJ.PankseppJ.CromwellH.C. (2012). Selective breeding for 50 kHz ultrasonic vocalization emission produces alterations in the ontogeny and regulation of rough-and-tumble play. — Behav. Brain Res. 229: 138-144.

WilladsenM.SefferD.SchwartingR.K.W.WöhrM. (2014). Rodent ultrasonic communication: male prosocial 50-kHz ultrasonic vocalizations elicit social approach behavior in female rats (Rattus norvegicus). — J. Comp. Psychol. 128: 56-64.

WilluhnI.ToseA.WanatM.J.HartA.S.HollonN.G.PhillipsP.E.M.SchwartingR.K.W.WöhrM. (2014). Phasic dopamine release in the nucleus accumbens in response to pro-social 50 kHz ultrasonic vocalizations in rats. — J. Neurosci. 34: 10616-10623.

YoungK.A.GobroggeK.L.WangZ. (2011). The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior. — Neurosci. Biobehav. Rev. 35: 498-515.

ZhangT.Y.ChretienP.MeaneyM.J.GrattonA. (2005). Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. — J. Neurosci. 25: 1493-1502.

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