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Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates
Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates
Andrew Bass2001, Brain Research Reviews
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Brain Research Reviews 35 (2001) 246–265
www.elsevier.com / locate / bres
Review
Social behavior functions and related anatomical characteristics of
vasotocin / vasopressin systems in vertebrates
James L. Goodson*, Andrew H. Bass
Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
Accepted 19 December 2000
Abstract
The neuropeptide arginine vasotocin (AVT; non-mammals) and its mammalian homologue, arginine vasopressin (AVP) influence a
variety of sex-typical and species-specific behaviors, and provide an integrational neural substrate for the dynamic modulation of those
behaviors by endocrine and sensory stimuli. Although AVT /AVP behavioral functions and related anatomical features are increasingly
well-known for individual species, ubiquitous species-specificity presents ever increasing challenges for identifying consistent structure–
function patterns that are broadly meaningful. Towards this end, we provide a comprehensive review of the available literature on social
behavior functions of AVT /AVP and related anatomical characteristics, inclusive of seasonal plasticity, sexual dimorphism, and steroid
sensitivity. Based on this foundation, we then advance three major questions which are fundamental to a broad conceptualization of
AVT /AVP social behavior functions: (1) Are there sufficient data to suggest that certain peptide functions or anatomical characteristics
(neuron, fiber, and receptor distributions) are conserved across the vertebrate classes? (2) Are independently-evolved but similar behavior
patterns (e.g. similar social structures) supported by convergent modifications of neuropeptide mechanisms, and if so, what mechanisms?
(3) How does AVT /AVP influence behavior — by modulation of sensorimotor processes, motivational processes, or both? Hypotheses
based upon these questions, rather than those based on individual organisms, should generate comparative data that will foster cross-class
comparisons which are at present underrepresented in the available literature. 2001 Elsevier Science B.V. All rights reserved.
Theme: Neural basis of behaviour
Topic: Neuropeptides and behaviour
Keywords: Vasopressin; Vasotocin; Vocalization; Evolution; Sex differences; Oxytocin
Contents
1. Introduction ............................................................................................................................................................................................
2. AVT /AVP brain distributions: conserved and divergent features, sexual dimorphisms, and steroid-mediated plasticity ....................................
2.1. Conserved neurochemical and anatomical features.............................................................................................................................
2.2. Species diversity in anatomical characteristics ...................................................................................................................................
2.3. Sex differences and sex steroid-mediated plasticity ............................................................................................................................
2.4. Glucocorticoid-mediated plasticity....................................................................................................................................................
3. AVT /AVP and behavior: general observations, sex differences and species specifity .....................................................................................
3.1. General behavioral characteristics.....................................................................................................................................................
3.2. Sex differences ...............................................................................................................................................................................
3.3. Species differences ..........................................................................................................................................................................
3.4. AVT /AVP and stress ........................................................................................................................................................................
4. Discerning evolutionary patterns: conservation, convergence, and a pluralistic neuroethological approach .....................................................
4.1. Conservation...................................................................................................................................................................................
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*Corresponding author. Present address: Department of Psychology, 0109, 9500 Gilman Dr., University of California, San Diego, La Jolla, CA 92093,
USA. Tel.: 11-858-822-4427; fax: 11-858-534-7190.
E-mail address: jgoodson@ucsd.edu (J.L. Goodson).
0165-0173 / 01 / $ – see front matter 2001 Elsevier Science B.V. All rights reserved.
PII: S0165-0173( 01 )00043-1
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
4.2. Vocal communication — a model case..............................................................................................................................................
4.3. Convergent behavior, convergent mechanisms? .................................................................................................................................
4.4. A pluralistic neuroethological approach ............................................................................................................................................
5. Conclusions ............................................................................................................................................................................................
Acknowledgements ......................................................................................................................................................................................
References...................................................................................................................................................................................................
1. Introduction
Regulation of vertebrate social behavior requires that
somatomotor expression be integrated with multiple coordinating influences, including sensory information from the
environment (e.g. social stimuli and seasonal cues) and
internal stimuli (e.g. endocrine state) [243]. In addition,
sensorimotor and physiological processes must be modulated in a highly specific manner to yield an appropriate
profile of complex sex-typical and species-specific behaviors. In a broad range of vertebrate species, arginine
vasotocin (AVT) and arginine vasopressin (AVP) have
emerged as key components of such complex coordinated
behavioral expression. As shown in Table 1, AVT /AVP
modulate a variety of social behaviors, and the behavioral
effects of peptide administration often vary between
species, gonadal sexes, and animals exposed to different
hormonal conditions. Furthermore, in several vertebrate
classes, divergence in social tactics is correlated with intraor interspecific divergence in the distribution of AVT /AVP
neural elements (also shown in Table 1). As shown in
Table 2, a variety of other anatomical findings also support
a role for AVT /AVP in the production of integrated social
behavior patterns, as AVT /AVP elements are often sexually
dimorphic, modulated by gonadal hormones, and sensitive
to changes in season or photoperiod.
Despite the broad diversity observed in AVT /AVP
distributions and functions, common patterns also emerge.
Hence, our fundamental purpose here is to extensively
overview the available literature, thereby providing a
foundation for the critical evaluation of evolutionary
conservation, divergence, and convergence in the anatomical and functional traits of AVT /AVP systems.
2. AVT /AVP brain distributions: conserved and
divergent features, sexual dimorphisms, and steroidmediated plasticity
2.1. Conserved neurochemical and anatomical features
Both AVT /AVP peptide structure and receptor structure
have been largely conserved throughout vertebrate evolution. Most vertebrate classes except mammals possess the
ancestral nine amino acid peptide form, i.e. AVT; AVP
differs only in position 3, with phenylalanine being
247
255
256
257
257
258
258
substituted for isoleucine. Silurid mammals have additionally substituted lysine for arginine in position 7 (lysine
vasopressin) [1]. Similarly, AVT receptors in teleost fish
and anuran amphibians are highly similar to the V1a
receptors of tetrapods. Thus, the V1a -like receptors of both
mammals and non-mammals are coupled to the inositol
phosphate second messenger system and exhibit strong
conservation in the amino acid sequences which are
proposed to be involved in peptide binding [154,169].
This conservation is paralleled in the basic features of
AVT /AVP neuron and fiber distributions. Table 3 provides
an overview of all vertebrate species for which wholebrain AVT /AVP-ir descriptions and chartings are available.
In all vertebrate species studied to date, magnocellular and
parvocellular AVT /AVP neurons are located in the preoptic
area-anterior hypothalamus (POA-AH; recognized as the
paraventricular and supraoptic cell groups of most tetrapods), and these cells project to other brain regions and to
the hypophysis (review: [165]). These characteristics are
found in both modern jawless and jawed vertebrates,
suggesting that they have been conserved for at least 500
million years. Similarly, basic AVT /AVP fiber distributions
observed for modern vertebrates were likely present prior
to tetrapod evolution. The available evidence for several
distantly related species of teleosts and elasmobranchs
reveals extensive similarities with the AVT /AVP-ir fiber
distributions described for tetrapods [112]. In virtually all
jawed vertebrates, AVT /AVP-ir fibers are located in the
POA, anterior and lateral hypothalamic areas, midbrain
tegmentum (typically including ventral, paralemniscal, and
dorsal tegmental areas), periaqueductal gray, a variety of
isthmal structures (e.g. nucleus isthmi and locus coeruleus)
and viscerosensory areas of the caudal medulla (e.g.
nucleus of the solitary tract and area postrema).
Tetrapod vertebrates exhibit additional derived anatomical characters that were established relatively early in
evolution and remain largely conserved. Particularly important for social behavior are the AVT /AVP cell groups of
the extended amygdala (i.e. lateral and medial amygdala of
amphibians and mammals, respectively, and the bed
nucleus of the stria terminalis; BNST; Table 1). These
neurons project to a variety of brain sites which are
likewise implicated in social behavior, including the lateral
septum, nucleus accumbens, amygdala, and periaqueductal
gray (see Refs. [112,165] and references in Table 3).
Proposed homologues of these brain regions also contain a
Fish
Vocalization
Amphibians
Birds
• Cynops pyrrhogaster (p.i.) [133]
Scent marking
• Porichthys notatus (POA-AH c , Teg)
[111,112]
Acris crepitans (p.i.; Ac d,e) [44,156,157]
Bufo americanus (p.i.) [201]
Bufo cognatus (p.i.) [188]
Hyla cinerea (p.i.b **) [180]
Hyla versicolor (p.i.) [202,214]
Rana catesbeiana (p.i.b,c **) [30,31]
Rana pipiens (p.i.b,c **) [68,69,190]
• Mesocricetus auratus (AH**, BNST, LS,
mPOA-AH b **, PAG**, VLH; AH; AH e)
[5–7,12,13,86–93,95,119,127,132,242]
• Saimiri sciureus (i.c.v.) [246]
• Suncus murinus (i.c.v.*) [198]
• Coturnix japonica (i.c.v.) [41]
• Serinus canaria (p.i.b ) [226]
• Spizella pusilla (S) [108]
• Zonotrichi leucophrys (i.c.v.*)
[155]
• Fundulus heteroclitus
(spawning reflex; p.i.**)
[144,153,182,244]
• Bufo americanus (phonotaxis; p.i.*) [199,200]
• Cynops pyrrhogaster (courtship, spermatophore
deposition; i.c.v., p.i.) [133]
• Rana catesbeiana (phonotaxis; p.i.*) [31]
• Rana pipiens (release calling; p.i.b,c **) [68,69,190]
• Taricha granulosa (approach; amplexus; i.c.v.b ,
Med.b , p.i.b **, dPOA, Inf, OT, CSF)
[33,166,168,196,213,261]
• Columba livia (combined sexual
behaviors; p.i.) [141]
• Coturnix japonica
(approach; copulation; p.i., i.c.v.)
[41]
• Gallus domesticus (combined
sexual behaviors; p.i.) [141]
• Rabbit spp., unspecified (copulation; p.i.) [140]
• Mesocricetus auratus (lordosis; mPOA-AH*) [127]
• Rattus spp. (cell firing in males prior to copulation;
lordosis; i.c.v.*, p.i.*; MeA; HYP*, SCN e *)
[159,163,204]
• Microtus ochrogaster (i.c.v.**; BNST g ) [43,236,247]
• Rattus spp. (SCN e) [207]
Pair-bonding and mate choice
Offensive aggression
• Rattus spp. (i.c.v.**, p.i.**) [248]
• Saimiri sciureus (i.c.v.) [246]
• Mesocricetus auratus (DMH h *) [58]
• Microtus ochrogaster (LS; BNST e , LH d , LS d , MeAe ,
PVN g **, SON g **) [14,15,232,234,238]
• Microtus montanus (PVN g *, SON g *) [238]
• Microtus pennsylvanicus (LH d ) [14]
• Rattus spp. (i.c.v.*) [179]
Parental behavior
Sexual behavior
(appetitive and
consummatory;
specified by case)
Mammals
• Spizella pusilla (S) [108]
• Taeniopygia guttata (S) [110]
• Uraeginthus granatina (S) [109]
• Homo sapiens (CSF**) [45]
• Mesocricetus auratus (mPOA-AH**, VLH b ; AH; AH e)
[61–63,87,94,96,187]
• Microtus ochrogaster (i.c.v.c **) [206,247,259]
• Rattus spp. (Amy b , i.c.v.b , LS, MeA; LS; BNST e , LS d )
[47,49,77,82,145,146,185]
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
•
•
•
•
•
•
•
248
Table 1
Social behavior functions of AVT /AVP as determined by exogenous peptide administration (site abbreviation in parentheses is given in plain text; intrasexual behavior correlation with -ir content (RIA)
or endogenous release / physiology (site in bolded text); intrasexual anatomical correlations (site in italicized text). Findings are for males unless otherwise denoted (*females; **males and females)a
• Mus spp. (p.i.b ) [27]
• Rattus spp. (DS, HP, i.c.v., LS, p.i.b,c **, SON; S)
[10,23–26,28,50,79,80,83,84,184,186,220]
Social recognition
• Oncorhynchus masou (ordinary vs.
precocious males; NPOm g ) [172]
• Porichthys notatus (polymorphic; diverge in parental,
spawning, courtship, nest defense and associated
vocalizations; POA-AH c **; POAe,f **) [99,111]
• Trimma okinawae (socially-mediated sex change;
POAf ) [117]
• Thalassoma bifasciatum (socially-mediated sex
change; NPOm) [104]
• Acris crepitans (non-calling satellite vs.
calling males; Ac d,e) [156]
• Emberizid / Estrildid spp.
(territorial vs. colonial; S)
[108–110]
• Microtus spp. (biparental, monogamous vs. no paternal care,
polygamous; BlAh **, BNST e,h , CA3 h , CeAh , Cer-M h , Cg h,i ,
CMT h , DB h,i , DG h , Gr h , H h , LDT h,i **, LHb h , LS c,h,i **,
MDT h , MeAe , MG h , MM h , nXII h , ncx h , NST h , PAG h , PFl h ,
PoT h , PTT h , PVN g **, PVT h , Rt h , SC h , SON g **, VMH h ,
VPT h,i , VS h) [131,230,238,240,259]
• Peromyscus spp. (biparental, monogamous vs. no paternal
care, polygamous; BNST d,e,f , DB h , LS h **, ncx h **, S-HP h **)
[22,129]
• Microtus /Peromyscus spp. (transgenic experiment; affiliative
behavior induction; i.c.v.; Cg h , Cla h , LDT h , VPT h) [255]
a
Abbreviations: Ac, nucleus accumbens; AH, anterior hypothalamus; Amy, amygdala; aPOA, anterior preoptic area; AVT, area ventralis of Tsai; B, basal nucleus of Meynert; BlA, basolateral
amygdala; BNST, bed nucleus of the stria terminalis; CA3, field CA3, stratum; CeA, central amygdala; Cer-M, cerebellum (molecular); Cg, cingulate cortex; Cla, claustrum; CMT, centromedial
thalamus; CSF, cerebrospinal fluid; DB, diagonal band; DCn, dorsal cochlear nucleus; DCtx, dorsal cortex; DD, dorsal diencephalon; DG, dentate gyrus; dPOA, dorsal preoptic area; DS, dorsal
septum; For., forebrain; Gr, granule cell layer (accessory olfactory); H, habenula; HP, hippocampus; HYP, hypothalamus; IC, inferior colliculus; i.c.v., intracerebroventricular; Inf, infundibulum; IP,
interpeduncular nucleus; LC, locus coeruleus; LCtx, lateral cortex; LDT, laterodorsal thalamus; LH, lateral hypothalamus; LHb, lateral habenula; LS, lateral septum; M, mammilary nuclei; MCtx,
medial cortex; MDT, mediodorsal thalamus; MeA, medial amygdala; Med., medulla; MG, medial geniculate; MM, medial mammilary nucleus; mPOA, medial preoptic area; mPOA-AH, medial
preoptic area-anterior hypothalamus; MPN, medial preoptic nucleus; MTu, medial tuberal nucleus; nXII, hypoglossal nucleus; ncx, neocortex; NPOm, magnocellular preoptic nucleus; NS, nucleus
sphericus; NTS, nucleus of the solitary tract; OT, optic tectum; PAG, periaqueductal gray; PFl, paraflocullus; p.i., peripheral injection; PM, premammilary nucleus; POA, preoptic area; POA-AH,
preoptic area-anterior hypothalamus; POA-LH, preoptic area-lateral hypothalamus; POM, medial preoptic nucleus; PoT, posterior thalamus; PT, paratenial thalamus; PTN, pretrigeminal nucleus; PTT,
PVT, paraventricular thalamus; R, raphe nuclei; RA, robust nucleus of the archistriatum; Rt, reticular nucleus; S, septum; S-HP, septo-hippocampal region; SC, superior colliculus; SCN,
suprachiasmatic nucleus; SDA, sexually dimorphic area; SFi, septofimbrial nucleus; sm, stria medullaris; SN, substantia nigra; SON, supraoptic nucleus; st, stria terminalis; SUM, supramammilary
nucleus; tc, tuber cinerum; Teg, midbrain tegmentum; TS, torus semicircularis; Tu, olfactory tubercle; V6, bed nucleus of the decussation of the fasciculus lateralis telencephali (Taricha); V12, pars
dorsalis hypothalami (Taricha); V13, posterior lobe of pars ventralis hypothalami (Taricha); V16, nucleus visceralis superior, nucleus isthmi region (Taricha); VLH, ventrolateral hypothalamus; VMH,
ventromedial hypothalamus; VMN, ventromedial nucleus of the hypothalamus; VP, ventral pallidum; VPT, ventroposterior thalamus; VS, ventral subiculum; VTA, ventral tegmental area; VTB, ventral
trapezoid body; ZI, zona incerta.
b
Function is modulated by steroid hormones or is seasonally variable.
c
Function is sexually diergic.
d
Behavior correlates with -ir fiber density.
e
Behavior correlates with -ir cell number.
f
Behavior correlates with -ir cell size.
g
Behavior correlates with peptide mRNA.
h
Behavior correlates with receptor binding.
i
Behavior correlates with receptor mRNA.
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
Divergent social strategies
(intraspecific and interspecific
differences; specified by case)
249
250
Table 2
AVT /AVP anatomical characteristics: sexual dimorphisms (anatomical sites in parentheses are shown in plain text); gonadal steroid / castration-sensitivity (sites in bolded text); seasonal / photoperiodic
variation (italicized text). Steroid / castration sensitivity and seasonal variation is for males unless otherwise denoted by asterisks (*females; **males and females)a
-ir cell number and/or cell size
-ir fiber density
Fish
• Oncorhynchus masou (POAe **) [172,173]
• Porichthys notatus (POA-AH e) [99]
• Trimma okinawae (POA) [117]
• Porichthys notatus (Teg) [112]
Amphibians
• Rana catesbeiana (Amy, SCN d ; PTN**) [36]
• Taricha granulosa (Amy, aPOA, BNST, V6 c,d ,
V12 c,d , V13 c,d , V16 c,d ) [167]
• Rana catesbeiana (Amy, H) [36]
•
•
•
•
Reptiles
• Coturnix japonica (POM, POM) [175]
• Gallus domesticus (Ac region d , BNST f , DD) [137,138]
• Serinus canaria (BNST, BNST**, BNST ) [227,228]
• Taeniopygia guttata (BNST; BNST**) [142]
• Coturnix japonica (LS, POM; BNST, LS, POM)
[9,175,176,222,223]
• Gallus domesticus (BNST, DD, LS f ) [137,138]
• Serinus canaria (DD, LS; DD**, LS**; BNST, LS)
[227,228]
• Taeniopygia guttata (BNST; BNST**) [142]
Mammals
• Callithrix jacchus (BNST) [235]
• Cavia porcellus (IC d , VTB d ) [75,76]
• Cricetus cricetus (LH, LS, MeA; DB, LH, LS, MeA,
PAG, HP, VTA; DB**, LH**, LS**, MeA**,
PAG**, HP**, VTA**) [39]
• Eliomys quercinus (LC, LH, LS, MeA, PAG, DB, HP,
VTA; DB**, LC**, LH**, LS**, MeA**, PAG**,
HP**, VTA** ) [120]
• Jaculus orientalis (BNST, MeA; BNST, MeA;
BNST, MeA) [147]
• Mesocricetus auratus (SON) [60]
• Microtus ochrogaster (BNST, MeA;
BNST, MeA) [230,232]
• Phodopus sungorus (BNST, MeA) [73]
• Rattus spp. (BNST d,f , BNST b , MeAd,f ; BNST,
MeA, SCN) [2,51,160,183,207,218,231]
• Cavia porcellus (DCn d , IC d , VTB d ) [75,76]
• Jaculus orientalis (BNST, DB, IP, LH, LS, MDT, MeA,
PAG, PTT, R, sm, st, SUM, tc; BNST, DB, IP, LH, LS,
MDT, MeA, PAG, PTT, R, sm, st, SUM, tc; BNST, DB,
IP, LH, LS, MDT, MeA, PAG, PTT, R, sm, st, SUM, tc) [147]
• Meriones unguiculatus (LS, SDA; LS**, SDA**) [48]
• Microtus spp. (LH, LS; LH, LS**) [14,151,232,237]
• Phodopus sungorus (LH, LS) [73]
• Rattus spp. (BNST, LH b , LS b , MeAb , PAG b , HP b ;
Amy**, B, DB**, HP, LC, LH**, LS**, PAG**, PM,
PVT, R, SFi, SN, SUM, Tu, VP, VTA, ZI)
[51–55,101,115,231]
Abbreviations as in Table 1.
Sex differences in steroid / castration sensitivity.
c
Seasonal / photoperiodic variation in sex differences.
d
Females.males.
e
Intrasexual morph differences.
f
Includes developmental comparisons (sub-adults).
b
Receptor binding (or mRNA if noted)
AVT/AVP mRNA
• Oncorhynchus keta (For., NPOm)
[124,171]
• Oncorhynchus masou (NPOm e **)
[172,173]
• Thalassoma bifasciatum (NPOm) [104]
• Rana catesbeiana (Amy, Dln d , OT, Teg;
Amy**, H**, OT b , PTN b , S**, TS b ) [32,35]
• Taricha granulosa (OT, Teg; dPOA, OT )
[35,65,260]
• Taricha granulosa (Amy**)
[34]
Anolis carolinensis (DCtx, LCtx, MCtx) [189]
Gekko gecko (LS, NS, PAG) [205,211]
Pseudemys scripta (Amy, LH, LS, PAG, SN, VTA) [203]
Python regius (Amy, LH, LS, PAG, SN, VTA) [203]
Birds
a
-ir content (RIA)
• Mesocricetus auratus (HYP) [60]
• Rattus spp. (LS, MeA) [55,116]
• Serinus canaria (AVT**, RA**)
[225]
• Coturnix japonica (BNST,POM) [174]
• Gallus domesticus (Ac region d , BNST, DD)
[137]
• Mesocricetus auratus (VLH;
BNST, MPN, POA-LH,
VLH**) [59,62,134,257]
mRNA in M. auatus: MPN [257]
• Mus musculus (mPOAd , M d ) [71]
• Peromyscus spp. (CMT d ) [129]
• Phodopus sungorus (MTu, PM,
VMN; VMN c , VMN** ) [73,74]
• Microtus spp. (BNST) [236]
• Rattus spp. (BNST f , MeAf ; BNST b **, MeA**,
PVN**) [38,70,160–162,183,208,209,212,215,
221,229,233]
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
Class
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
Table 3
Species for which whole-brain descriptions and chartings of AVT /AVP-ir
are available
Agnathans
Hagfish
Lampreys
Eptatretus stouti a [170]
Lampetra fluviatilis a [113]
Cartilaginous fish
Sharks
Scyliorhinus caniculus a [216]
Bony fish
Teleosts
Lungfish
Amphibians
Anurans
Urodeles
Caecilians
Reptiles
Turtles
Lizards,
snakes
Birds
Mammals
Rodents
Primates
a
b
Poecilia latipinna a [21]
Porichthys notatus [112]
Salmo gairdneri a [217]
Protopterus aethiopicus b [114]
Bufo japonicus [135]
Rana catesbeiana [36]
Rana ridibunda [105]
Xenopus laevis [106]
Pleurodeles waltlii [105]
Taricha granulosa [152]
Typhlonectes compressicauda [107]
Typhlonectes natans [123]
Pseudemys scripta [203]
Anolis carolinensis [189]
Gekko gecko [205,211]
Python regius [203]
Junco hyemalis [177]
Serinus canaria [143]
Taeniopygia guttata [224]
Cavia porcetella [76]
Jaculus orientalis [147]
Meriones unguiculatus [253]
Mesocricetus auratus [72]
Rattus spp. [54]
Macaca fascicularis [40]
Little detail is provided for the brainstem.
Not a whole brain description (only data for this group).
modest AVT-ir fiber innervation in fish, although the
source of these fibers is in the POA.
2.2. Species diversity in anatomical characteristics
Despite the general similarity of AVT /AVP systems
described above, major species differences are observed
for multiple AVT /AVP elements. Most pronounced are
variations in the brain distributions and abundance of the
V1a receptor sub-type in mammals (lack of sufficient data
precludes similar assessments in other vertebrate classes).
The V1a receptor mediates AVP’s behavioral effects and its
distribution is essentially unique in all species examined to
date (e.g. [129,131,256,259]). Although most species
exhibit at least a limited amount of binding in areas
implicated in social behavior (see above for relevant brain
251
regions), large quantitative differences exist which have
been strongly linked to divergent patterns of social behavior (see Ref. [255] and next section).
Similarly, large species differences are also observed in
the locations of AVT /AVP-ir perikarya and / or AVT /AVP
mRNA, with up to 19 cell groups being exhibited in a
single species (Taricha granulosa [152,165]). Expansion
of the AVT systems appears to have accompanied the
water-to-land transition, an observation consistent with
AVT /AVP’s roles in hydromineral balance [165,261].
Potentially important for the expression of social behavior
are species differences in the presence or absence of
AVT /AVP cells in the medial amygdala (or its non-mammalian homologues), and the presence or absence of a
dense AVT /AVP-ir fiber plexus in the lateral septum. This
latter feature is present in most vertebrates species examined to date, but absent in T. granulosa, Mesocricetus
auratus, and primates (see references above). Interestingly,
Mesocricetus and primates do contain AVP receptors in the
lateral septum [72,256], and AVP binding in this site is
required for hamsters to display normal levels of flank
marking (Table 1). Thus, these observations strongly
suggest that behavioral actions of AVT /AVP may occur via
paracrine peptide action [237].
Finally, species differences also exist with regard to the
presence or absence of intraspecific variation, particularly
sex differences and steroid sensitivity in AVT /AVP distributions. These features are discussed below.
2.3. Sex differences and sex steroid-mediated plasticity
As shown in Table 2, the abundance of AVT /AVP
elements in a number of brain areas are sexually dimorphic
(virtually always male.female), regulated by gonadal
hormones, and sensitive to changes in season and / or
photoperiod. Most extensively studied with regard to these
variables are mammals, which exhibit marked species
differences [254]. It should be noted that the limited
representation of some species in the table is a result of
negative findings for sexual dimorphism and not a lack of
investigation (hamster, M. auratus [4,72]; marmoset, Callithrix jacchus [235,239]; rhesus monkey, Macaca spp.
[40,256]); primates have not been examined for steroid or
seasonal sensitivity. In addition, early reports from other
species may have failed to reflect existing anatomical
characteristics due to the technical difficulties of staining
the extended amygdala cells. Nonetheless, strong similarities do exist between some very distantly related
species, with multiple vertebrate classes exhibiting sex
dimorphisms and steroid sensitivities for AVT /AVP neural
elements in the septum, BNST, periaqueductal gray,
amygdala, and POA-AH (Table 2). Determining which of
these features are conserved or convergent is difficult, and
complicated by the fact that rigorous methods of quantification have not been consistently employed across species.
In general, sexually dimorphic or seasonally variable
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features are also testosterone (T)-dependent (i.e. T increases expression; a large number of examples are given
in Table 2), but the relative contributions of T metabolites
have been investigated in only a few representative
species. In gonadectomized rats, AVP mRNA expression in
the medial amygdala and BNST is most sensitive to
estradiol (E) plus dihydrotestosterone (DHT); E is relatively effective alone, whereas DHT alone has no effect
[56,233]. Sex differences in AVP-ir and mRNA are not due
to differential levels of circulating steroids in adulthood, as
they persist following gonadectomy and steroid treatment.
Rather, findings for the BNST indicate that sex differences
in mRNA expression and steroid sensitivity are organized
by T in early development [229]. Similarly, AVT-ir sex
differences in Japanese quail (Coturnix japonica; see Table
2) are organized prior to hatching and are accompanied by
sexually-different sensitivities to T in adulthood. Treatment of eggs with E produces female-typical levels of
AVT-ir in male quail, while treatment with an aromatase
inhibitor produces male-typical AVT-ir levels in female
quail [175]. Thus, aromatization of T is likely an important
factor in the sexual differentiation of the quail AVT
system. As determined by radioimmunoassay, steroid
sensitivities in the bullfrog (Rana catesbeiana) are somewhat different, with gonadectomized animals showing
stronger responses to DHT than E in multiple brain areas
[32].
2.4. Glucocorticoid-mediated plasticity
A limited amount of data in mammals now also demonstrate that AVP elements are sensitive to glucocorticoids,
thus providing a potential mechanism for the dynamic
modulation of social behavior by the presence of stressors.
Glucocorticoid feedback modulates AVP mRNA and V1a
receptor binding in the neurosecretory hypothalamus and
other forebrain regions; effects may differ between brain
regions and also between sexes (e.g. [85,178,197,
221,241]).
3. AVT /AVP and behavior: general observations, sex
differences and species specifity
3.1. General behavioral characteristics
As shown in Table 1, AVT /AVP modulate a wide variety
of social behaviors. These behaviors include both olfactory
(scent marking) and vocal communication, sexual behavior, pair-bonding, parental behavior, offensive aggression, and social recognition. Note that the categories are
necessarily somewhat contrived, as they are in reality
extensively overlapping (e.g. vocalization and sexual behavior). In many species, peptide effects are sexually
different and / or sensitive to levels of steroid hormones
(also shown in Table 1). The central behavioral actions of
AVT /AVP are mediated by the V1a receptor sub-type in
mammals or a similar receptor in non-mammals (e.g.
[41,111]), and are largely independent of peptide pressor
functions [57,84,204].
In addition to the social behaviors shown in Table 1,
AVT /AVP influence learning and memory functions
[57,81,148] and other behaviors which are not primarily
social, including hibernation [121,122], sleep site investigation in fish [149], locomotion in amphibians [29],
grooming behavior (e.g. [132,219]) and exploratory / anxiety-related behavior in rodents (e.g. [8,84,126,150]).
Some of these behavioral functions are species-specific and
may be evolutionarily derived from more general AVT /
AVP functions. For instance, AVP’s general role in mammalian thermoregulation [16] likely set the stage for its
subsequent and more derived role in hibernation [121].
Similarly, fluctuations in central and / or plasma AVT /AVP
levels are extensively linked to parturition and oviposition
across the tetrapod classes (review: [164]), and speciesspecific behaviors related to oviposition are likewise
modulated by AVT, including egg-laying movements in
amphibians [168] and vertical tree-climbing in reptiles
[118].
3.2. Sex differences
In general, AVT /AVP is more extensively associated
with male behavior than with female behavior, although
this may partially reflect an emphasis on behaviors which
are exhibited only by males (e.g. mate calling). A particularly informative example is therefore provided by
studies of bullfrogs, in which AVT effects on male-specific
behavior (mate calling), female-specific behavior (mate
call phonotaxis), and behavior common to both sexes
(release calling) were examined. AVT facilitates phonotaxis in females and mate calling in males [31], but produces
opposite effects on release calling in males and females
(facilitates and inhibits, respectively); effects are produced
in a seasonally-variable manner [30]. Furthermore, only
female bullfrogs beyond the tadpole stage exhibit increased
locomotion in response to AVT administration [29], consistent with AVT’s modulation of female-typical phonotaxis.
Peptide effects on other behaviors can be much more
strongly sex-specific, as in cases where only males are
behaviorally dependent on AVT /AVP (e.g. social discrimination in rats [23]). In contrast, females are occasionally
found to be behaviorally insensitive to AVT /AVP but
sensitive to oxytocin-like peptides (see below). Importantly, oxytocin plays a role in numerous aspects of female
reproductive physiology and maternal behavior (reviews:
[249,258]); thus, whereas AVT /AVP modulate a variety of
behaviors exhibited only by males, oxytocin is extensively
linked to female-specific functions [254].
A striking example of sex-specific peptide functions is
provided by studies of pair-bond formation in the monogamous prairie vole (Microtus ochrogaster). Partner preference in male voles is dependent upon AVP [247],
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
whereas oxytocin, and not AVP, is required for preference
formation in females [130,245]. Although these studies
demonstrate sex differences in the necessity of endogenous
peptides for normal pair-bond formation (determined by
delivery of peptide antagonists), a recent study demonstrates that either peptide may nonetheless facilitate preference in both male and female voles [43]. These findings
therefore suggest that sex-specific requirements for AVP or
oxytocin are associated with sex differences in endogenous
peptide release. This is particularly interesting, given that
species differences in the presence or absence of pair-bond
behavior are produced almost exclusively by postsynaptic
mechanisms, as discussed in the next section.
Similarly strong sex differences in vasopressin–oxytocin
function have now also been found for the polymorphic
plainfin midshipman fish [111], although peptide functions
in this case are associated with divergent social tactics and
not with gonadal sex per se. Differential useage of
vocalization between the midshipman morphs is tied to the
differential expression of parental behavior, nest defense,
and courtship. All adult morphs give agonistic ‘grunts,’
whereas only the courting male morph gives trains of
grunts, courtship ‘hums’ and ‘growls’ [19,37]. Vocal-motor
activity elicited by electrical stimulation of the POA-AH
(predominantly grunt-like) is inhibited by local AVT
administration in the courting male morph, whereas isotocin (homologue of oxytocin) is ineffective. This peptide
sensitivity is reversed in females, similar to the sexspecific functions of AVP and oxytocin in voles. However,
sneak-spawning males, which are female-typical in numerous vocal characteristics, share the isotocin-sensitivity of
females and are insensitive to AVT. Thus, sex differences
in AVT function in the midshipman are dissociated from
gonadal sex, suggesting that gonadal and peptidergic
characteristics are independently differentiated and are
potentially visible to natural selection as individual phenotypic characters. Whether the pattern of sex differences
obtained for midshipman and the prairie vole is generally
observed in vertebrates remains to be determined.
3.3. Species differences
The extensive association of AVT /AVP with intraspecific behavioral variation suggests that the process of
natural selection may also lead to interspecific divergence
in behavior via modifications of peptidergic mechanisms
[100]. This hypothesis is now supported by representative
data from across the vertebrate classes. Thus, whereas
AVT /AVP facilitate most of the male behaviors shown in
Table 1, similar behaviors in other species may be
inhibited; inhibited behaviors include aggression in some
songbirds (see below), sexual and vocal behavior in
Japanese quail [41], and vocalization in fish [111,112].
Alternatively, AVT /AVP may promote behavior in one
species and produce no effect in a closely related species,
as shown for the behavior of Microtus voles. Some
microtine vole species are highly affiliative, monogamous,
253
and exhibit biparental care (e.g. prairie voles), whereas
other species in the genus are relatively asocial, nonmonogamous, and exhibit no paternal care (e.g. montane
voles, M. montanus) [258]. In male prairie voles, AVP
promotes a number of behaviors characteristic of its
species’ social structure, including partner preference and
affiliation, paternal behavior, and selective post-mating
aggression [43,234,247,255]. In contrast, similar behaviors
are not promoted by AVP administration in the nonmonogamous montane vole [255,259]. These species differences in behavior and peptide sensitivity are correlated
with a variety of differences in the distribution of AVP
elements, including receptor binding, receptor mRNA,
peptide mRNA, and AVP-ir (Table 1).
Divergence in AVP receptor distribution among Microtus species appears to be the most important factor
associated with differences in monogamous and nonmonogamous behavior, as suggested by a recent transgenic
experiment [255]. Monogamous vole species (M. ochrochaster and M. pinetorum) possess a 428-base pair sequence
in the 59 flanking region of the V1a receptor gene that is not
present in non-monogamous congeners (M. montanus and
M. pennsylvanicus). Receptor distribution in transgenic
mice (expressing a prairie vole V1a receptor mini-gene
containing a 2.2-kb segment of the 59 flanking region) is
highly similar to the prairie vole and affiliative behavior is
likewise induced by exogenous AVP in transgenic mice,
but not wild-type conspecifics.
Social structure additionally correlates with qualitatively
different AVT functions in colonial and territorial male
songbirds. Infusions of AVT into the septum facilitate
overt aggression in the colonial zebra finch (Estrildidae:
Taeniopygia guttata; a gregarious, group-breeding species)
[110], whereas similar infusions inhibit aggression in the
territorial field sparrow (Emberizidae: Spizella pusilla)
[108]. AVT also inhibits aggression in the territorial violeteared waxbill (Estrildidae: Uraeginthus granatina) [109], a
species which likely evolved a territorial social structure
independently of the field sparrow. The violet-eared waxbill is more closely related to the colonial zebra finch than
to the field sparrow, and is virtually identical to the zebra
finch in important aspects of social structure (e.g. biparental behavior and mating system) and ecological
variables relevant to AVT function (e.g. osmoregulatory
and thermoregulatory challenges). Thus, numerous potential confounds are controlled for in this species comparison, indicating that variability in AVT’s behavioral
effects are related to species divergence in territorial and
colonial behavior. Interestingly, AVT /AVP facilitates aggression in both affiliative bird and vole species, while
producing qualitatively different effects in related asocial
species (see above).
3.4. AVT /AVP and stress
Comparative findings strongly support the idea that the
ancestral AVT system of vertebrates was comprised of cell
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groups in the POA-AH which projected to the pituitary and
other brain regions (see General anatomical features
above). Across vertebrate classes, modern homologues of
these cell groups play important roles in neuroendocrine
responses to stress (particularly to social, psychological
and emotional stressors; e.g. [3,194,195,252]), and AVT /
AVP and corticotropin releasing factor (CRF) synergize to
regulate adrenocorticotropin release [11,193]. Similarly,
synergistic effects of AVP and CRF are found for social
behavior modulation by the amygdala [77].
Although glucocorticoid feedback modulates AVP
mRNA and V1a receptor binding (e.g. [85,178,197,
221,241]; see Glucocorticoids and AVP above), very little
study has been conducted to determine whether and how
glucocorticoid levels may impact on AVT /AVP behavioral
modulation. One of the few examples is provided in prairie
voles. Stress and exogenous corticosterone inhibit pairbonding in female prairie voles, whereas stress facilitates
bonding in males [66,67]. Given the strong sex differences
in vasopressin–oxytocin modulation of pair-bonding in this
species [130,247], it appears likely that steroid–neuropeptide interactions contribute to the divergence between
males and females. Intrasexual behavior may also be
differentiated by interactions between AVP and stress, as
differential exposure to social subjugation during puberty
produces individual variation in the aggressive behavior of
male Syrian hamsters; this variation is correlated with
vasopressin content in the anterior hypothalamus [63].
Importantly, glucocorticoids may dynamically modify
the polarity of neuropeptide effects within individuals, as
shown for amplexus-related medullar neuron activity in
male newts [196]. In this case, whether AVT facilitates or
inhibits neuronal activity is dependent upon the temporal
juxtaposition of corticosterone and AVT delivery.
4. Discerning evolutionary patterns: conservation,
convergence, and a pluralistic neuroethological
approach
Given the diversity of roles that AVT /AVP play in
species-specific behaviors, a critical question to be answered is whether AVT /AVP distributions and social
behavior functions may be conceptualized in a manner that
is broadly relevant. Evolutionary lability in AVT /AVP
systems makes this question particularly salient, as a
‘model system’ approach is simply not tenable. Thus,
peptide mechanisms found to underlie territoriality, monogamy, or vocal behavior in one species cannot be assumed
to underlie similar behaviors in other species which have
evolved the behavior independently. With this in mind, we
address several questions below which we regard as
critical if the study of AVT /AVP systems is to advance
from a collection of individual findings to a comparative
database which allows broadly meaningful extrapolation:
(1) Are there sufficient data to suggest that certain peptide
functions or anatomical characteristics are conserved across the vertebrate classes? (2) How do AVT /AVP influence behavior across vertebrate groups — by modulation of sensorimotor processes, motivational processes, or
both? (3) Are independently-evolved but similar behavior
patterns (e.g. similar social structures) supported by convergent modifications of neuropeptide mechanisms, and if
so, what mechanisms? Finally, we describe a pluralistic
neuroethological approach [18] which should greatly increase the power of future studies of social behavior and
AVT /AVP. This approach, which presents existing
phenotypes as products of multiple interacting mechanisms, may be viewed as a framework within which the
above questions may be most usefully answered.
4.1. Conservation
At present, comparative data are more extensive for
behaviorally-relevant anatomical features than for social
behavior functions per se. Hence, while consistent patterns
are readily recognized for some anatomical traits, causal
linkages to behavioral functions are more difficult to
discern. As discussed earlier, parvocellular AVT /AVP
populations in the POA-AH are present across all vertebrate groups, and tetrapods also exhibit parvocellular AVT /
AVP cell groups within the extended amygdala. These
parvocellular cell groups comprise the conserved core of
behaviorally-relevant AVT /AVP distributions and give rise
to basal forebrain projections in most species thus far
examined (amygdala / BNST, septum, and POA-AH; see
references in first section of this review and Table 3). In
addition, AVT /AVP elements in these regions are sexually
dimorphic and sensitive to gonadal hormones across
multiple vertebrate classes (Table 2). Hence, the widespread presence of sexual dimorphism in the extended
amygdala cell groups and their projections likely represent
a conserved trait for tetrapod vertebrates, and non-dimorphism in some species likely represents a derived
character state. A similar case may be tentatively hypothesized for the steroid sensitivity of these projection systems, although much more data are required.
Characteristics of the AVT /AVP magnocellular systems
are quite different. Sexual dimorphism is only infrequently
observed (e.g. [60,104]) and is therefore likely convergent.
Furthermore, although anatomical features do in some
cases parallel intraspecific, interspecific, and seasonal
differences in social behavior ([104,167,171,172,238]; see
Table 1), the lack of central projections from these neurons
suggest that they do not modulate behavior directly.
Rather, magnocellular systems may modulate peripheral
physiology via the hypophysis in a manner appropriate for
the expression of certain behaviors, such as parental urine
ingestion in rodents [238]. Thus, behaviorally-relevant
characteristics of AVT /AVP magnocellular populations are
most likely species-specific and not conserved, although
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
further research may reveal convergent patterns of magnocellular function associated with convergence in physiological demands of behavior.
Importantly, although the presence of AVT /AVP in a
given region may be suggestive of particular functions, the
actual relationships between AVT /AVP distributions and
behavior will be strongly influenced by receptor distributions, which are evolutionarily labile. This observation
may help explain why the kinds of behaviors which are
influenced by AVT /AVP are similar across vertebrate taxa,
while the polarity of AVT /AVP effects (i.e. facilitation or
inhibition) may differ even between closely related species
[109,259]. Similarly, while the presence of sexual dimorphism in AVT /AVP distributions suggests that sex
differences in peptide function may exist in some form or
another, the exact neuromodulatory and behavioral differences produced by such dimorphisms remain unclear.
Thus, a question critically in need of further research is
whether sex differences in the distribution of peptide
elements may be consistently related to differences in
peptide behavioral function; this may be determined by
exogenous peptide administration into specific neural loci
or by the use of behaviorally relevant anatomical techniques (e.g. combined histochemistry for immediate early
genes and neuropeptides). As discussed earlier, sex differences in AVT /AVP function are in some cases qualitative
[23,111,130], but the small number of relevant studies
precludes any general conclusions.
Indeed, hypotheses about conservation in AVT /AVP
social behavior functions are substantially constrained by
the limited number of behaviors which have been examined across a sufficient number of vertebrate groups. No
data are yet available in reptiles for any of the behaviors
covered in Table 1, and multiple types of behavior have
been examined only in a single vertebrate class. With the
exception of vocalization, which is discussed below,
comparisons across several classes are possible only for
sexual behavior, although data on overt aggression are also
available for mammals and birds. Both appetitive and
consummatory aspects of male sexual behavior are influenced by AVT /AVP in at least three vertebrate classes
(only two classes for females; see Table 1), suggesting that
AVT /AVP modulation of male sexual approach and copulation may be evolutionarily conserved, at least for tetrapods (spawning behavior elicited by peripheral AVT
administration in fish is not evoked by central peptide
administration; for discussion see Ref. [181]). Finally,
overt aggression is noteworthy as the only behavior to be
influenced by comparable site-specific AVT /AVP administrations (septum) across different vertebrate classes, although this is currently known only for songbirds (e.g.
[108]) and rodents [145]. Similar investigations in additional species would therefore yield important information
about the functional significance and evolution of AVT /
AVP projections into the septum, which are anatomically
conserved (see above).
255
4.2. Vocal communication — a model case
Any determination of whether phylogenetically widespread peptide functions represent conservation or convergence is critically dependent upon assessments of how the
peptides actually influence behavior. For those behaviors
which have evolved independently in multiple evolutionary
clades (e.g. vocal communication), this question is particularly salient, as outlined below.
Vocal modulation is the most widely established behavioral role for AVT /AVP (Table 1) and this is paralleled
by AVT /AVP-ir fiber distributions in vocally-active regions
across a broad range of vertebrate taxa (see AVT /AVP
brain distributions above). Electrical brain stimulation
evokes vocalizations from a number of homologous neural
sites in mammals (review: [136]), anuran amphibians
(review: [78]), birds (review: [46]), fish [64,97,112], and
reptiles [139]. These sites include the septum and
amygdala (or homologues in fish), POA-AH, and
periaqueductal gray. In addition, AVT /AVP fibers are
found in paralemniscal / dorsal tegmental regions which are
implicated in vocal-acoustic integration in fish [20,112],
bats [158], and birds [42]. Local AVT administration
modulates vocalization in a number of these sites in birds
(septum) [108] and fish (POA-AH; paralemniscal tegmentum) [111,112]. AVT /AVP vocal modulation may therefore
occur by influences on sensorimotor processes, motivation
processes or both, and may be convergent or conserved, as
summarized in the four hypotheses below.
Hypothesis 1: Despite the independent evolution of
vocalization in a number of vertebrate lineages [17], the
integrative brain regions involved may play more broad
and evolutionarily conserved roles in the social communication of all vertebrate species, regardless of communication modality. For instance, the vocally-active regions
discussed above map quite closely to regions in which
AVP modulates scent marking in hamsters [12,92]; also see
Table 1). Therefore, although AVT /AVP modulation of
vocalization across vertebrate taxa is not a homologous
condition as a vocal function of AVT /AVP, it may nonetheless be homologous as a communicative function of AVT /
AVP.
Hypothesis 2: Convergent vocal functions of AVT /AVP
may be related to conserved roles for these peptides in
functionally-related motivational systems which influence
somatomotor systems on a more general level (e.g.
modulatory systems which broadly influence agonistic,
sexual, or affiliative behaviors). Table 1 shows several
cases that may support this argument, with some vertebrate
groups exhibiting peptide roles in vocal modulation that
are paralleled by influences on other related behaviors. For
instance, AVT /AVP influences both territorial song and
overt aggression in birds [108], affiliative behavior and
vocalizations associated with social isolation in mammals
[248,255], and mate calling and other sexual behaviors in
amphibians [31,166]. Thus, AVT /AVP modulation of vocal
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behaviors may be homologous between taxa as an agonistic, affiliative, or sexual peptide function, but not necessarily as a communicative function.
Hypothesis 3: AVT /AVP may play more targeted and
conserved roles in sensorimotor processes associated with
audition, as suggested by the phylogenetically widespread
presence of AVT /AVP in vocal-acoustic brain regions (see
above). Hence, peptide influences on vocalization would be
homologous as a sensorimotor function of AVT /AVP.
Hypothesis 4: Finally, AVT /AVP vocal functions in
different vertebrate taxa may be convergent, with peptidergic influences on sensorimotor processes, relevant motivational processes or both evolving independently.
Distinguishing between these four hypotheses is crucial,
as accurate distinction will provide important information
about how AVT /AVP systems interface with somatomotor
systems, and will allow a determination of whether behaviors may be modulated by these peptides specifically
and independently, or only as part of broader behavioral
domains. A clear resolution is not possible at present.
However, AVT /AVP modulation of a number of behaviors
appears to occur via effects on sensorimotor processes
[26,81,213], suggesting that peptides may act upon
stimulus cue acquisition rather than motivational processes
per se. This has been explicitly demonstrated for male
rough-skinned newts, in which AVT’s modulation of
appetitive approach is limited to sexual stimuli when all of
the stimuli tested are olfactory (e.g. appetitive response to
food odors are not affected by AVT), but is not limited to
sexual stimuli in the visual modality [213]. Thus, in this
case AVT acts upon sensorimotor integration in a
modality-specific manner, suggesting that more global
motivational processes are not the primary targets of
peptide action.
The Thompson and Moore experiments [213] are the
only studies to date which have explicitly addressed the
issue of how AVT /AVP influence social behavior, and far
more data are required to determine the generality of their
findings. However, as is clear from our hypotheses above,
determining the primary targets of AVT /AVP action (i.e.
motivational or sensorimotor processes) is of the upmost
importance in constructing informative evolutionary
schemes.
4.3. Convergent behavior, convergent mechanisms?
In generating a broad conception of AVT /AVP functions, perhaps the most difficult question to be addressed is
whether evolutionary convergence in particular behavioral
characteristics is reliably associated with convergence in
peptide mechanisms. More plainly, this question asks to
what extent findings from one species may yield accurate
predictions for others.
As presented earlier, available evidence in birds suggests that independent evolution of a territorial social
structure is associated with convergent evolution in the
polarity of septal AVT’s effects on overt aggression in
males, controlling for multiple other aspects of behavior
and ecology [108–110]. Thus, on a functional level,
convergence in social spacing (exclusive territoriality vs.
coloniality) is in fact associated with convergence in
AVT’s behavioral functions. However, no anatomical data
are yet available which might suggest how convergence is
reflected at the level of neural mechanisms.
Most extensively examined for such structure–function
correlations are a variety of arvicoline rodents of the
genera Microtus (vole) and Peromyscus (mouse). Species
within each genus differ in mating system and amount of
paternal care, and multiple species comparisons within
each genus yield consistent correlations between social
structure and V1a receptor distributions [22,129,131,
240,259]. In each species comparison, differences are
found for binding within the lateral septum, a structure
which has been implicated in paternal behavior [234].
However, the relationship between binding and social
structure is reversed for the two rodent genera. Similarly,
within each genus a weaker relationship exists between
mating system and AVP-ir cell number in the BNST
[14,22,230] (although significant species differences are
not consistently found [237]), but the relationship is again
reversed between genera.
Although these findings suggest that similar peptide
mechanisms are not reliably associated with independently
evolved social behavior characteristics in Microtus and
Peromyscus, it should be noted that for each species pair
studied, the species differ in more respects than mating
system and biparental care. Hence, the anatomical differences between species may be more reliably associated
with some other aspect of behavior or ecology. One
variable proposed to account for the pattern of findings is
species-typical levels of aggression [22], although assessing this hypothesis is at present difficult due to limited
relevant, comparable data and a few somewhat inconsistent
findings [22,259].
Based on the findings in songbirds [108–110], we have
therefore asked whether the anatomical differences found
between rodent species may more consistently correlate
with social spacing patterns. Within Microtus, monogamous pairs of M. ochrogaster and M. pinetorum exhibit a
high degree of home range overlap with other adult
conspecifics (facultatively in M. ochrogaster), whereas the
non-mongamous comparison species M. montanus and M.
pennsylvanicus occupy much more exclusive ranges (although exclusive ranges in M. pennsylvanicus are found
more often for females, with males exhibiting extensive
range overlap) [103,125,210,250]. In Peromyscus, this
relationship between home range overlap and monogamy /
biparental care is reversed, with monogamous pairs of P.
californicus occupying virtually exclusive ranges while the
non-monogamous P. leucopus and P. maniculatus exhibit
variable spacing that occasionally produces very high
densities of overlapping adult ranges [191,251]. The
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
correlations between anatomical characteristics and species
differences in social structure are therefore largely consistent between rodent genera if the behavioral variable
considered is social spacing, with the caveat that species
comparisons are complicated by the temporal and conditional dynamics of spacing (see next section). Hence, for
each species comparison of AVP anatomical characteristics
that has been conducted in Microtus and Peromyscus, the
species which occupies a more exclusive home range
exhibits a higher density of V1a receptor binding in the
lateral septum and a greater number of AVP-ir neurons in
the BNST (if cell number differences are present)
[14,22,129,131,230,240,259]. Interestingly, in most of
these cases, the species with the more exclusive home
range also occupies an average range of greater absolute
size than the comparison species (see references above).
These observations therefore suggest that species differences in AVP anatomy may extensively reflect spacing
behavior. That V1a receptor binding within the lateral
septum is the most consistently found anatomical difference is also noteworthy, as the connectivity of the lateral
septum in multiple vertebrate taxa suggests a role for this
region in the integration of social and spatial cues
[98,192].
Importantly, this hypothesis is not inconsistent with the
assertion that patterns of V1a receptor binding play a
critical role in determining whether a species exhibits
monogamous or non-monogamous behavior [254]. Rather,
our hypothesis suggests that species differences in receptor
binding within the lateral septum may be more reliably
associated with social spacing than with mating system
(which may be more strongly correlated with AVP receptor
distributions in other brain areas). Indeed, transgenic
experiments clearly demonstrate the importance of receptor
distributions for the expression of monogamous or nonmonogamous behavior, but also demonstrate that binding
levels within the lateral septum are not a predictor of
whether AVP is effective in facilitating affiliative behaviors
associated with monogamy [255].
Whether our spacing hypothesis is accurate in predicting
correlated convergence in behavior and anatomy in rodents
remains to be fully determined. However, the fact that this
hypothesis renders the available rodent dataset internally
consistent, and that it suggests a similarity to behavioral
data in songbirds, raises the exciting possibility that
behavior and AVT /AVP mechanisms / functions may indeed
evolve in concert across a wide phylogenetic spectrum.
This proposal is strengthened by the observation that in
both birds and voles, AVT /AVP administrations influence
aggression in qualitatively different ways between species
with high home range overlap versus those with little
overlap — aggression is facilitated in those species with
high overlap (the colonial zebra finch and the prairie vole)
[110,247,259] and inhibited or unaffected in species with
more exclusive territories (field sparrow, violet-eared
waxbill and montane vole) [108,109,259].
257
4.4. A pluralistic neuroethological approach
In answering the above questions, it is of critical
concern that comparisons of any data incorporate (or
control for) all relevant variables. Although neurobiologists
tend to explain existing phenotypes in terms of structure–
function relationships, existing phenotypes are in fact the
product of multiple variables, including behavioral characters, structural characters, and ecological environment. As
presented by Bass [18], each of these factors may be
viewed as a circle of a Venn diagram, with overlap between
all of the circles representing the existing phenotype, and
overlap between pairs of circles representing mechanisms
which influence the phenotype (behavioral–ecological,
structural–behavioral, and ecological–structural mechanisms). Importantly, only a portion of each circle actively
influences the phenotype at any given time, thus as the
circles rotate over time (e.g. seasonally, over sequential life
history stages, or over evolutionary history), the phenotype
will change as a product of dynamic modification of
mechanisms. This pluralistic approach makes evident a
potentially dangerous pitfall — that failure to consider all
relevant characters and life history information may promote ‘random’ error and misinterpretation of data, as
ignored factors may extensively modify the variables under
consideration.
Given the temporally and evolutionarily dynamic nature
of AVT /AVP systems, a pluralistic neuroethological approach is particularly critical. The need for a pluralistic
approach is especially evident with regard to considerations of AVT /AVP and spacing behavior, given that
spacing behavior overlaps and interacts with virtually
every other behavioral character, is extensively influenced
by ecological environment, and is highly labile over days,
seasons, life histories and evolution [102,128,210]. Thus,
these dynamics suggest that simple relationships between
individual behavioral characters and AVT /AVP structure
and / or social behavior functions may not exist; this is a
concern which likely applies to all of the topics covered in
this review. Hence, questions about broad patterns in
AVT /AVP social behavior characteristics and related
anatomy will be most powerful and usefully guided by a
pluralistic approach.
5. Conclusions
The comprehensive overview presented here of AVT /
AVP behavioral functions and related anatomical features
suggests some extensive similarities between vertebrate
groups, particularly with regard to the distribution of AVT /
AVP-ir cells and fibers, sexual behavior functions, and
modulation of vocalization. Furthermore, data from a
variety of songbirds and arvicoline rodents suggest that
septal AVT /AVP may exert phylogenetically widespread
influences on social spacing and aggression, with indepen-
258
J.L. Goodson, A.H. Bass / Brain Research Reviews 35 (2001) 246 – 265
dent and convergent evolution of spacing patterns being
reliably associated with convergent patterns of peptide
function and / or V1a receptor binding within the lateral
septum. In general, the broad similarities in AVT /AVP cell
and fiber distributions appear to provide a basis for the
modulation of comparable classes of behavior across
vertebrate taxa, although exact peptide functions and the
polarity of behavioral influence may potentially differ
between sexes and species as a function of multiple
dynamic influences. These include evolutionary lability in
receptor distributions and sensitivity of AVT /AVP neural
elements to gonadal and adrenal steroids. Steroid sensitivities and sexual dimorphisms are observed in multiple
species for the AVT /AVP cells of the extended amygdala
and their projections, but the relationships of these characteristics to site-specific neurobehavioral function largely
remain to be determined. Bridging this gap between
anatomy and function should be a major focus of future
research, and such investigations are necessary across a
number of vertebrate groups before broadly meaningful
conclusions may be drawn. Other issues of fundamental
importance also remain virtually unexplored, including the
question of how AVT /AVP influence behavior — by
modulation of sensorimotor processes, motivational processes, or both. Answering this question for multiple
species will allow a determination of whether behaviors
may be modulated independently and specifically, or only
as part of broader behavioral domains, and will provide an
essential framework for comparing peptide behavioral
functions across taxa. It remains equally important to
identify how AVT /AVP modulates neurophysiological
processes and thereby social behavior functions, as we
have begun to address for specific neural loci in the
midshipman fish [111,112]. Overall, we have here identified many informational gaps, but the data also provide
substantial indications that AVT /AVP behavioral functions
and related anatomical characteristics can indeed be conceptualized in ways that are phylogenetically broad while
at the same time informative for the diversity of speciesspecific traits that are influenced by AVT and AVP.
However, this conceptualization will require the augmentation of standard neurobiological paradigms by a pluralistic
neuroethological approach [18] — one which recognizes
not only the importance of structural and behavioral
characters, but of life history and ecological variables as
well.
Acknowledgements
The authors thank Elizabeth Adkins-Regan for encouraging this project. Support for this publication was
provided by NIH postdoctoral grant F32 NS-0443 to J.L.
Goodson, and NIH grant DC 00092 and NSF grant IBN
9987341 to A.H. Bass.
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