Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution.

Testosterone (T) regulates many traits related to fitness, including aggression. However, individual variation in aggressiveness does not always relate to circulating T, suggesting that behavioural variation may be more closely related to neural sensitivity to steroids, though this issue remains unresolved. To assess the relative importance of circulating T and neural steroid sensitivity in predicting behaviour, we measured aggressiveness during staged intrusions in free-living male and female dark-eyed juncos (Junco hyemalis). We compared aggressiveness to plasma T levels and to the abundance of androgen receptor (AR), aromatase (AROM) and oestrogen receptor alpha (ORα) mRNA in behaviourally relevant brain areas (avian medial amygdala, hypothalamus and song control regions). We also asked whether patterns of covariation among behaviour and endocrine parameters differed in males and females, anticipating that circulating T may be a better predictor of behaviour in males than in females. We found that circulating T related to aggressiveness only in males, but that gene expression for ORα, AR and AROM covaried with individual differences in aggressiveness in both sexes. These findings are among the first to show that individual variation in neural gene expression for three major sex steroid-processing molecules predicts individual variation in aggressiveness in both sexes in nature. The results have broad implications for our understanding of the mechanisms by which aggressive behaviour may evolve.

Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches.

Dopamine (DA) is produced in numerous brain areas and influences a wide variety of social behaviors, but very few data are available to establish the socially-relevant response properties of most DA populations, which comprise eight cell groups numbered A8-A15. Anatomically, these DA populations are evolutionarily conserved, and all have been identified in both birds and mammals. We now report the Fos responses of tyrosine hydroxylase-immunoreactive (TH-ir; putatively dopaminergic) neurons in the A8-A15 cell groups of male zebra finches following exposure to a control condition or one of six different social stimuli: a heterospecific male, conspecific male, fighting in a mate competition paradigm (which includes both male and female stimuli), a courtship interaction without physical contact, a courtship interaction with physical contact but no mounting, and a courtship interaction with mounting. We found that the DA cell groups exhibit distinctive profiles of responsiveness to social stimuli. Fos induction in A8, A9, A10 and midbrain A11 neurons increased significantly in response to a variety of conspecific stimuli, but not heterospecific stimuli. In contrast, Fos induction in the preoptic A14 neurons was observed specifically in response to sexual interactions, and Fos induction in hypothalamic A11 neurons appears to primarily reflect the performance of courtship singing. Infundibular A12 neurons, which may be involved in stress-related processes, showed the highest level of TH+Fos colocalization in control subjects. This colocalization decreased in response to all conspecific stimuli except fighting, and did not decrease following exposure to a heterospecific male.

Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates.

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.

Vasotocin innervation and modulation of vocal-acoustic circuitry in the teleost Porichthys notatus.

Arginine vasotocin (AVT) and its mammalian homologue arginine vasopressin (AVP) modulate reproduction-related and other social behaviors in a broad range of vertebrate species. These functions of AVT/AVP may be in part achieved through the modulation of sensorimotor integration, although experimental evidence supporting this hypothesis remains limited. In the present experiments, we demonstrate (1) AVT innervation of candidate vocal-acoustic brain regions, and (2) AVT modulation of vocal-motor physiology in the plainfin midshipman fish (Porichthys notatus), which uses vocalizations in both mate attraction and agonistic contexts. AVT distribution was compared with known vocally active brain regions and to central auditory and vocal pathways. AVT-immunoreactive fibers and putative terminals descend almost exclusively from the preoptic area and are found in two primary candidate sites for vocal-acoustic integration - the anterior tuberal hypothalamus and paralemniscal midbrain tegmentum. AVT immunoreactivity is also located in several other vocally active regions, including the ventral tuberal nucleus, periaqueductal gray, and paraventricular regions of the isthmus and rostral hindbrain. The parvocellular preoptic area itself is also vocally active, although thresholds are substantially higher than for other regions. The functional significance of AVT input to vocal-acoustic regions was demonstrated in the paralemniscal midbrain where local delivery of AVT modulated electrically evoked, rhythmic vocal-motor output, which precisely mimicked natural vocalizations. AVT produced dose-dependent inhibitions of parameters associated with call initiation (burst latency and number of vocal-motor bursts elicited) but not of vocal-motor patterning (fundamental frequency and burst duration). Together, these findings provide support for the proposal that AVT modulates sensorimotor processes underlying social/acoustic communication.

Rhythmic midbrain-evoked vocalization is inhibited by vasoactive intestinal polypeptide in the teleost Porichthys notatus.

Vasoactive intestinal polypeptide (VIP) is distributed in vocal midbrain areas of multiple vertebrate taxa, suggesting that VIP may modulate midbrain-evoked vocalization. To test this hypothesis, neurophysiological experiments were conducted in the teleost Porichthys notatus which generates vocalizations in mating and agonistic contexts. Electrical stimulation of the paralemniscal midbrain and local delivery of VIP were conducted in conjunction with occipital nerve recordings that reflect the patterned output of hindbrain vocal circuitry. Consistent with our hypothesis, VIP significantly reduced the duration and number of rhythmic vocal-motor bursts obtained in a dose-dependent manner; vocalization latency was concomitantly increased. These results provide the first evidence for VIP modulation of midbrain vocal function.

Forebrain peptides modulate sexually polymorphic vocal circuitry.

The peptide arginine-vasopressin (mammals) and its evolutionary precursor arginine-vasotocin (non-mammals) modulate reproductive physiology and numerous related social behaviours, as do oxytocin (mammals) and its homologues mesotocin and isotocin (fish). The distributions in the brain and/or the behavioural functions of these peptides often differ between the sexes, and between species with divergent social structures. Here we present neurophysiological evidence that males with vocal characteristics typical of females share a pattern of neuropeptide function with females rather than conspecific males. The plainfin midshipman fish (Porichthys notatus) has two male morphs with different reproductive tactics and vocalizations (a key species-typical behaviour which varies in its physical attributes and contextual usage, depending on the morph's social strategy). Forebrain-evoked, rhythmic vocal-motor activity that precisely mimics natural vocalizations was modulated by arginine-vasotocin, isotocin and their antagonists delivered to the preoptic area-anterior hypothalamus, a primary site for behavioural integration in all vertebrates. Peptides had different effects in males that acoustically court females (arginine-vasotocin-sensitive) than in females and sneak-spawning males (isotocin-sensitive), showing that the neuromodulatory mechanisms that establish reproduction-related behaviour can be dissociated from gonadal sex.

Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla)

The present investigation assessed the effect of lesions of the septum on male courtship and aggression in the territorial field sparrow (Spizella pusilla) and the colonial zebra finch (Taeniopygia guttata). In addition, pair-bonding and a variety of other social behaviors were examined in the zebra finch and dawn song (both the strictly agonistic song type and the multipurpose song type) was examined in the field sparrow. Zebra finches were tested in three phases both before and after receiving bilateral electrolytic lesions of the septum or sham surgery. These phases were: (1) competition tests in which a subject and a stimulus male were exposed to a female in an adjacent cage; (2) sexual behavior tests with a female; and (3) 10-day group cage tests in which subjects were in a mixed-sex environment. Aggressive behaviors (chases, threats, beak fences and pecks) were significantly reduced by septal lesions but not by sham surgery. Directed song (courtship) was significantly reduced in sexual behavior tests, with similar trends in other testing phases. Male field sparrows were tested 2 days pre-surgery and 2 days post-surgery in outdoor aviaries placed in their natural habitat. Tests consisted of dawn song observations and observations of courtship and aggression following introduction of a female to the subject's aviary, which was followed 10 min later by the introduction of another male (without removing the female). Septal lesions significantly facilitated both overt aggression (chases) and the number of simple (multi-purpose) songs. These results provide evidence that the septum participates in the regulation of male aggression and song in songbirds, and further suggest that variations in septal function may exist between territorial and colonial species.

Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla)

The present investigation assessed the effect of lesions of the septum on male courtship and aggression in the territorial field sparrow (Spizella pusilla) and the colonial zebra finch (Taeniopygia guttata). In addition, pair-bonding and a variety of other social behaviors were examined in the zebra finch and dawn song (both the strictly agonistic song type and the multipurpose song type) was examined in the field sparrow. Zebra finches were tested in three phases both before and after receiving bilateral electrolytic lesions of the septum or sham surgery. These phases were: (1) competition tests in which a subject and a stimulus male were exposed to a female in an adjacent cage; (2) sexual behavior tests with a female; and (3) 10-day group cage tests in which subjects were in a mixed-sex environment. Aggressive behaviors (chases, threats, beak fences and pecks) were significantly reduced by septal lesions but not by sham surgery. Directed song (courtship) was significantly reduced in sexual behavior tests, with similar trends in other testing phases. Male field sparrows were tested 2 days pre-surgery and 2 days post-surgery in outdoor aviaries placed in their natural habitat. Tests consisted of dawn song observations and observations of courtship and aggression following introduction of a female to the subject's aviary, which was followed 10 min later by the introduction of another male (without removing the female). Septal lesions significantly facilitated both overt aggression (chases) and the number of simple (multi-purpose) songs. These results provide evidence that the septum participates in the regulation of male aggression and song in songbirds, and further suggest that variations in septal function may exist between territorial and colonial species.

Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata).

The present experiments were conducted to test the hypothesis that septal arginine vasotocin (AVT) and vasoactive intestinal polypeptide (VIP) modulate directed song (a courtship behaviour) and aggression in male zebra finches (Taeniopygia guttata). Subjects were surgically fitted with a guide cannula directed at the septum. Following recovery they were tested for aggression and directed song following infusions of AVT, its antagonist (anti-vasopressin, AVP), and saline volume control. Infusion of the AVT antagonist significantly reduced all three aggressive behaviours measured (pecks, beak fences and chases); and AVT infusion significantly facilitated beak fencing. Vasoactive intestinal polypeptide treatment significantly reduced pecking. No treatment produced a change in directed song. Comparison with findings in mammals suggests that modulation of aggression by septal AVT (or AVP) is evolutionarily conserved in vertebrates, but modulation of aggression by VIP has not previously been reported for any vertebrate.

Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla).

Previous experiments demonstrate that lesions of the septum produce opposite effects on intraspecific male aggression in the territorial field sparrow (Spizella pusilla) and the colonial zebra finch (Taeniopygia guttata; facilitate vs inhibit, respectively) and intraseptal infusions of arginine vasotocin (AVT) and vasoactive intestinal polypeptide (VIP) modulate aggression in the male zebra finch (facilitate and inhibit, respectively). The present experiments were conducted to test the hypotheses that (1) septal AVT and VIP modulate both overt territorial aggression and the production of territorial song during the dawn chorus in male field sparrows and (2) these neuropeptides will exert effects opposite of those observed in the zebra finch, consistent with the prediction that social organization is associated with septal neuropeptide function. Wild-caught male field sparrows were fitted with chronic guide cannulae directed at the septum and were tested in outdoor aviaries placed in their natural habitat. Intrusion tests (introduction of a stimulus male) and dawn song observations were conducted following infusion of AVT, VIP, or saline control. Consistent with predictions, infusion of AVT significantly inhibited chases and significantly increased chase latency. No significant effects of VIP on chasing or chase latency were observed, although most subjects were more aggressive following infusion of VIP. Both AVT and VIP produced significant, selective effects on the complex (agonistic) song type (facilitation and inhibition, respectively) and produced no effect on the simple (multipurpose) song type. Thus, song and overt aggression appear be modulated independently by septal neuropeptides, and septal AVT and VIP function may differ between species which differ in the expression of territorial or colonial social organizations.

Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina).

Previous research demonstrates that intraseptal administrations of arginine vasotocin (AVT) inhibit male aggression in the territorial field sparrow (Emberizidae: Spizella pusilla) but facilitate aggression in the colonial zebra finch (Estrildidae: Taeniopygia guttata). In order to determine whether this difference may be related to the territorial and colonial social organizations of these two species, the effect of AVT infusions was examined in a territorial Estrildid species, the violet-eared waxbill (Uraeginthus granatina). This species is more closely related to the zebra finch than to the field sparrow and shares most critical features of breeding ecology in common with zebra finches, but differs in social organization. AVT infusions administered via chronic guide cannulae directed at the septum significantly inhibited aggressive behavior, consistent with results in the territorial field sparrow, supporting the hypothesis that social organization is correlated with AVT function. Similar experiments with mesotocin and substance P produced no effects on any of the behaviors measured, but infusions of vasoactive intestinal polypeptide (VIP) significantly facilitated aggression. This result contrasts with the inhibitory effect of septal VIP obtained in the colonial zebra finch, suggesting that VIP function may be correlated with social organization as well.

Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals.

Nucleus taeniae (Tn) is a prominent cell group within the medial archistriatum of birds. Based upon similarities in sex-steroid binding sites, this nucleus has been hypothesized to be homologous to the medial nucleus of the amygdala (Me) in mammals, which is known to modulate the expression of sexual behavior in rodents. We therefore tested whether or not Tn likewise plays a role in the expression of sexual behavior in male Japanese quail. We found that bilateral damage to Tn produced deficits in several components of male responses toward female stimuli that were indicative of decreased sexual arousal, including goal-oriented responses, vocalizations associated with courtship, and motor reflexes that precede copulation. Our results suggest that Tn influences a wide range of behavioral functions in response to sexual stimuli, and they indicate a function for this nucleus similar to that subserved by the Me in mammals. These results strengthen the argument that these sex-steroid accumulating cell groups are homologous and suggest a conservation of function for them despite the vastly divergent evolutionary histories separating birds and mammals.