The vertebrate social behavior network: evolutionary themes and variations

Abstract

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.

Figure 1

The social behavior network as originally suggested for mammals (schematics modified from Newman, 1999). The network is comprised of six nodes – the extended medial amygdala (i.e., the medial amygdala and the medial bed nucleus of stria terminalis, BSTm), the lateral septum (LS), the preoptic area (POA), the anterior hypothalamus (AH), the ventromedial hypothalamus (VMH) and various areas of the midbrain, including the periaqueductal gray. Each of the nodes binds sex steroid hormones and has been implicated in the control of multiple forms of social behavior. Newman (1999) proposes that this network does not contain segregated, linear systems for each kind of behavior. Rather, as shown in these schematic representations of immediate early gene data, each behavioral context is associated with a distinct pattern of activation across the nodes.

Figure 2

Connectional, functional and histochemical features of the social behavior network as exemplified in a vocalizing fish, the plainfin midshipman (Porichthys notatus). A. A schematic sagittal view of the midshipman brain. Electrical stimulation of numerous brain sites activates the hindbrain vocal pattern generator and elicits fictive vocal-motor output that precisely mimics natural vocalizations (shown here are fictive agonistic grunts). Tract tracings of vocally-active sites demonstrate that reciprocal connections exist between four areas (shown in red) that are homologous to nodes of the mammalian social behavior network (see Table 1). These areas are also reciprocally connected with nuclei of the basal telencephalon that are homologous to the septum and amygdala (shown in black; for clarity, connections are not shown). As with the six nodes of the mammalian social behavior network, these six areas express sex steroid receptors (e.g., Forlano et al., 2005). B. Neurons and fibers immunoreactive for arginine vasotocin (red) and isotocin (green) in the parvocellular preoptic area of the midshipman fish (DAPI counterstain is pseudocolored purple). These neurons are the evolutionary precursors of peptidergic neurons in the paraventricular hypothalamus of tetrapods (see panel C for evolution of the vasotocin-like peptide forms; schematic after Acher, 1972). In all vertebrates, these neurons project to components of the social behavior network, and in the midshipman, these projection systems modulate vocal-motor activity in a sex- and morph-specific manner (see text section on “Blending the sexes”). Scale bar in B =200 μm (modified from Goodson et al., 2003). Other abbreviations: AH, anterior hypothalamus; AT, anterior tuberal nucleus of the hypothalamus; PAG, periaqueductal gray; PL, paralemniscal tegmentum; POA, preoptic area; VMH, ventromedial hypothalamus; Vs, supracommissural nucleus of the ventral telencephalon; Vv, ventral nucleus of the ventral telencephalon.

Figure 3

Chemoarchictural themes of the social behavior network as exemplified in songbirds (photomontage of a female zebra finch brain at the level of the anterior commissure; AC). Immunohistochemical triple-labelling for vasoactive intestinal polypeptide (VIP; Alexa Fluor 488, green), neuropeptide Y (NPY; Alexa Fluor 594, red) and tyrosine hydroxylase (TH; Alexa Fluor 350, pseudocolored purple) shows the location of multiple zones of the lateral septum (LS) and bed nucleus of the stria terminalis (BST) that are now known to be extensively comparable to mammals (see Aste et al., 1998; Goodson et al., 2004a; Richard et al., 2004). This labeling also clearly shows the medial and lateral divisions of the ventromedial hypothalamus (i.e., VMH core and shell, respectively), which exhibit a similar topography across the vertebrate taxa (see Table 1). Scale bar = 200 μm. Modified from Goodson et al., 2004a. Other abbreviations: AH, anterior hypothalamus; BSTm, medial bed nucleus of the stria terminalis; BSTl, lateral bed nucleus of the stria terminalis; Hp, hippocampus; LSc, caudal division of the lateral septum (dorsal, ventrolateral, lateral and ventral zones denoted as LSc.d, LSc.vl, LSc.l and LSc.v, respectively); LSr, rostral division of the lateral septum; ME, median eminence; MS, medial septum; MSib, internal band of the medial septum; ot, optic tract; OM, occipitomesencephalic tract; PVN, paraventricular nucleus of the hypothalamus; SH, septohippocampal septum; v, lateral ventricle.

Figure 4

Functional themes of the lateral septum (LS) as exemplified by findings in wild-caught, territorial male song sparrows (Melospiza melodia; A-B) and field sparrows (Spizella pusilla; C-D). Similar to rodents, Fos-immunoreactive (-ir) cell counts in the ventrolateral LS are increased by an agonistic encounter (A; simulated territorial intrusion; STI), but the most aggressive animals show virtually no Fos induction (B; cf. Kollack-Walker and Newman, 1997). The aggression measure shown in B is based on contacts with the wire barrier that separated the subject from the intruder (data in A and B are from Goodson et al., submitted-a). Also similar to rodents, septal infusions of arginine vasotocin (AVT; homologue of arginine vasopressin) facilitate agonistic communication (C-D; cf. Irvin et al., 1990). Data shown in C-D are from field sparrows housed on semi-natural territories (field-based flight cages placed in natural habitat; modified from Goodson, 1998a). C. The number of simple and complex songs given spontaneously during the dawn singing period; these song types are multipurpose and strictly agonistic, respectively (see Nelson and Croner, 1991). D. The ratio of complex to simple songs, showing an increase in the agonistic content of song following intraseptal infusion of 100 ng AVT. *p<0.05, unpaired t-test (A) or Wilcoxon signed ranks (C-D).

Figure 5

A schematic representation of immediate early gene responses (Fos and/or Zenk) within the social behavior network following exposure to a same-sex conspecific in four estrildid songbird species that differ selectively in their species-typical group sizes (two colonial species, one modestly gregarious species and one territorial species; both males and females were examined). Exposure was conducted in a paradigm that limits overt behavioral performance, thus species differences should reflect differences in motivational and/or perceptual processes. Modified from Goodson et al., 2005.