James L. Goodson

The Vertebrate Social Behavior Network: Evolutionary Themes and Variations

Based on a wide variety of data, it is now clear that birds and teleost (bony) fish possess a core social behavior network within the basal forebrain and midbrain that is homologous to the social behavior network of mammals. The nodes of this network are reciprocally connected, contain receptors for sex steroid hormones, and are involved in multiple forms of social behavior. Other hodological features and neuropeptide distributions are likewise very similar across taxa. This evolutionary conservation represents a boon for experiments on phenotypic behavioral variation, as the extraordinary social diversity of teleost fish and songbirds can now be used to generate broadly relevant insights into issues of brain function that are not particularly tractable in other vertebrate groups. Two such lines of research are presented here, each of which addresses functional variation within the network as it relates to divergent patterns of social behavior. In the first set of experiments, we have used a sexually polymorphic fish to demonstrate that natural selection can operate independently on hypothalamic neuroendocrine functions that are relevant for (1) gonadal regulation and (2) sex-typical behavioral modulation. In the second set of experiments, we have exploited the diversity of avian social organizations and ecologies to isolate species-typical group size as a quasi-independent variable. These experiments have shown that specific areas and peptidergic components of the social behavior network possess functional properties that evolve in parallel with divergence and convergence in sociality.

Effects of central vasotocin and mesotocin manipulations on social behavior in male and female zebra finches.

Male and female zebra finches (Taeniopygia guttata; total n = 40) were fitted with chronic guide cannulae directed at the lateral ventricle and were tested for aggression, affiliation, and partner preference following infusions of mesotocin (MT), vasotocin (VT), their antagonists, and vehicle control. Aggressive behavior was tested in a mate competition paradigm and tests of intersexual affiliation and partner preference were conducted following 1 day of cohabitation with an opposite-sex individual. These tests also provided data on male courtship singing. The results demonstrate a modest dose-dependent facilitation of aggression by VT, but not MT, in both male and female finches. However, only males were sensitive to infusions of a vasopressin antagonist, suggesting that endogenous VT is more important for behavioral modulation in males. Peptide effects were specific to aggression, as no treatments influenced intersexual affiliation, partner preference, or male courtship singing. Thus, in contrast to rodents, partner preference is not readily induced by VT or MT in this species. However, the potential necessity of endogenous VT and MT for natural pair-bond formation remains to be tested.

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.

Neuro-evolutionary patterning of sociality

Evolutionary shifts in species–typical group size (‘sociality’) probably reflect natural selection on motivational processes such as social arousal, approach–avoidance, reward, stress/anxiety and dominance. Using four songbird species that differ selectively in sociality (one territorial, one modestly gregarious, and two highly gregarious species), we here examined immediate early gene (IEG) responses of relevant brain regions following exposure to a same–sex conspecific. The paradigm limited behavioural performance, thus species differences should reflect divergence in motivational and/or perceptual processes. Within the extended medial amygdala (which is involved in appetitive approach, social arousal and avoidance), we observed species differences in IEG response that are negatively graded in relation to sociality. In addition, brain areas that are involved in social stress and dominance–related behaviour (ventrolateral septum, anterior hypothalamus and lateral subdivision of the ventromedial hypothalamus) exhibited IEG responses that dichotomously distinguish the territorial species from the three gregarious species. The IEG responses of areas involved in reward (nucleus accumbens and ventral pallidum) and general stress processes (e.g. paraventricular hypothalamus, lateral bed nucleus of the stria terminalis and most areas of the lateral septum) do not correlate with sociality, indicating that social evolution has been accompanied by selection on a relatively discrete suite of motivational systems.

Putative isotocin distributions in sonic fish: Relation to vasotocin and vocal–acoustic circuitry

Recent neurophysiological evidence in the plainfin midshipman fish (Porichthys notatus) demonstrated that isotocin (IT) and arginine vasotocin (AVT) modulate fictive vocalizations divergently between three reproductive morphs. To provide an anatomical framework for the modulation of vocalization by IT and to foster comparisons with the distributions of the IT homologues mesotocin (MT) and oxytocin (OT) in other vertebrate groups, we describe putative IT distributions in the midshipman and the closely related gulf toadfish, Opsanus beta. Double‐label fluorescent histochemistry was used for IT and AVT (by using antibodies for MT, OT, and the mammalian AVT homologue, arginine vasopressin [AVP]). MT/OT‐like immunoreactive (MT/OT‐lir) cell groups were found in the anterior parvocellular, posterior parvocellular, and magnocellular preoptic nuclei. MT/OT‐lir fibers and putative terminals densely innervated the ventral telencephalon and numerous areas in the hypothalamus and brainstem. These distributions included all sites of vocal–acoustic integration recently identified for the forebrain and midbrain and diencephalic components of the ascending auditory pathway. Results were qualitatively comparable across morphs, species, and seasons. In contrast to the widespread distribution of MT/OT‐lir, AVP‐lir somata, fibers, and putative terminals were almost completely restricted to vocal–acoustic regions. These data parallel previous descriptions of AVT immunoreactivity in these species, although the present methods showed a previously undescribed, seasonally variable AVP‐lir cell group in the anterior tuberal hypothalamus, a vocally active site and a component of the ascending auditory pathway. These findings provided anatomic support for the role of IT and AVT in the modulation of vocal behavior at multiple levels of the central vocal–acoustic circuitry. J. Comp. Neurol. 462:1–14, 2003.

Chemoarchitectonic subdivisions of the songbird septum and a comparative overview of septum chemical anatomy in jawed vertebrates.

Available data demonstrate that the avian septal region shares a number of social behavior functions and neurochemical features in common with mammals. However, the structural and functional subdivisions of the avian septum remain largely unexplored. In order to delineate chemoarchitectural zones of the avian septum, we prepared a large dataset of double‐, triple‐, and quadruple‐labeled material in a variety of songbird species (finches and waxbills of the family Estrildidae and a limited number of emberizid sparrows) using antibodies against 10 neuropeptides and enzymes. Ten septal zones were identified that were placed into lateral, medial, caudocentral, and septohippocampal divisions, with the lateral and medial divisions each containing multiple zones. The distributions of numerous immunoreactive substances in the lateral septum closely match those of mammals (i.e., distributions of met‐enkephalin, vasotocin, galanin, calcitonin gene‐related peptide, tyrosine hydroxylase, vasoactive intestinal polypeptide, substance P, corticotropin‐releasing factor, and neuropeptide Y), enabling detailed comparisons with numerous chemoarchitectonic zones of the mammalian lateral septum. Our septohippocampal and caudocentral divisions are topographically comparable to the mammalian septohippocampal and septofimbrial nuclei, respectively, although additional data will be required to establish homology. The present data also demonstrate the presence of a medial septal nucleus that is histochemically comparable to the medial septum of mammals. The avian medial septum is clearly defined by peptidergic markers and choline acetyltransferase immunoreactivity. These findings should provide a useful framework for functional and comparative studies, as they suggest that many features of the septum are highly conserved across vertebrate taxa. J. Comp. Neurol. 473:293–314, 2004.

Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes

Neuroendocrine factors that produce species differences in aggregation behavior (sociality) are largely unknown, although relevant studies should yield important insights into mechanisms of affiliation and social evolution. We here focused on five species in the avian family Estrildidae that differ selectively in their species-typical group sizes (all species are monogamous and occupy similar habitats). These include two highly gregarious species that independently evolved coloniality; two territorial species that independently evolved territoriality; and an intermediate, modestly gregarious species that is a sympatric congener of one of the territorial species. Using males and females of each species, we examined binding sites for (125)I-vasoactive intestinal polypeptide (VIP), (125)I-sauvagine (SG; a ligand for corticotropin releasing factor, CRF, receptors) and a linear (125)I-V(1a) vasopressin antagonist (to localize receptors for vasotocin, VT). VIP, CRF and VT are neuropeptides that influence stress, anxiety and/or various social behaviors. For numerous areas (particularly within the septal complex), binding densities in the territorial species differed significantly from binding in the more gregarious species, and in most of these cases, binding densities for the moderately gregarious species were either comparable to the two colonial species or were intermediate to the territorial and colonial species. Such patterns were observed for (125)I-VIP binding in the medial bed nucleus of the stria terminalis, medial septum, septohippocampal septum, and subpallial zones of the lateral septum; for (125)I-SG binding in the infundibular hypothalamus, and lateral and medial divisions of the ventromedial hypothalamus; and for the linear (125)I-V(1a) antagonist in the medial septum, and the pallial and subpallial zones of the caudal lateral septum. With the exception of (125)I-SG binding in the infundibular hypothalamus, binding densitites are positively related to sociality.

Neural responses to territorial challenge and nonsocial stress in male song sparrows: segregation, integration, and modulation by a vasopressin V1 antagonist

The present experiments were conducted to determine (1) which basal forebrain regions and/or their peptidergic components are responsive to social challenge and nonsocial stress, and (2) the influence of an arginine vasopressin V(1) antagonist (AVPa) on these responses. Experiments were conducted in wild-caught male song sparrows (Melospiza melodia) that were housed on seminatural territories (field-based flight cages). Subjects were each fitted with a chronic guide cannula directed at the lateral ventricle and exposed to one of five conditions before sacrifice and histochemistry: saline + simulated territorial intrusion (STI; consisting of song playback and presentation of a caged conspecific male), AVPa + STI, saline + empty cage, AVPa + empty cage, unhandled. Two tissue series were prepared and immunofluorescently double-labeled for ZENK (egr-1) protein and either arginine vasotocin (AVT; avian homologue of AVP) or corticotropin releasing factor (CRF). The results indicate that the neuronal populations that are sensitive to nonsocial stress (capture, handling and infusion) and STI are at least partially segregated. Increases in ZENK-immunoreactive (-ir) nuclei following handling and infusion were observed in a large number of areas, whereas neural responses that were specific to STI were more limited. However, multiple areas showed responses to both handling and STI. AVPa infusions significantly reduced or eliminated most experimental increases in ZENK-ir, suggesting a broad role for endogenous AVT in the modulation of baseline activity and/or stress responsivity, and a much more limited role in the specific response to social challenge. Particular attention is given to the numerous zones of the lateral septum (LS), which are differentially responsive to handling, STI, and V(1)-like receptor blockade. These data suggest that septal AVT modulates neural responses to general stressors, not social stimuli specifically. Thus, species differences in septal AVT function (as previously described in songbirds) likely reflect differences in the relationship of stress or anxiety to species-specific behaviors, or to behavior in species-typical contexts.

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

Ever since investigations in the field of behavioral endocrinology were hatched with experiments on roosters, birds have provided original insights into issues of fundamental importance for all vertebrate groups. Here we focus on more recent advances that continue this tradition, including (1) environmental regulation of neuroendocrine and behavioral systems, (2) steroidogenic enzyme functions that are related to intracrine processes and de novo production of neurosteroids, and (3) hormonal regulation of neuroplasticity. We also review recent findings on the anatomical and functional organization of steroid-sensitive circuits in the basal forebrain and midbrain. A burgeoning body of data now demonstrates that these circuits comprise an evolutionarily conserved network, thus numerous novel insights obtained from birds can be used (in a relatively straightforward manner) to generate predictions for other taxa as well. We close by using birdsong as an example that links these areas together, thereby highlighting the exceptional opportunities that birds offer for integrative studies of behavioral neuroendocrinology and behavioral biology in general.