Septal lesions and aggressive behavior

doi:10.1016/S0091-6773(77)92407-5

Behavioral Biology

Volume 21, Issue 1, September 1977, Pages 157-161

https://doi.org/10.1016/S0091-6773(77)92407-5 Get rights and content

Attack behaviors of dominant colony males of established albino rat colonies, on intruders, were measured following septal lesions or control operations. Septal damage produced a significant decrease in piloerection, biting, and lateral attack behaviors, as well as in the number of wounds observed on the intruders. These differences tended to disappear during a 3-week period after surgery. Thus septal damage in the rat as well as the mouse appears to produce a systematic reduction in aggressive attack behaviors.

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Most animals encounter social challenges throughout their lives as they compete for resources. Individual responses to such challenges can depend on social status, sex, and community-level attributes, yet most of our knowledge of the behavioral and physiological mechanisms by which individuals respond to challenges has come from dyadic interactions between a resource holder and a challenger (usually both males). To incorporate differences in individual behavior that are influenced by surrounding group members, we use naturalistic communities of the cichlid fish, Astatotilapia burtoni, and examine resident dominant male responses to a territorial intrusion within the social group. We measured behavior and steroid hormones (testosterone and cortisol), and neural activity in key brain regions implicated in regulating territorial and social dominance behavior. In response to a male intruder, resident dominant males shifted from border defense to overt attack behavior, accompanied by decreased basolateral amygdala activity. These differences were context dependent – resident dominant males only exhibited increased border defense when the intruder secured dominance. Neither subordinate males nor females changed their behavior in response to a territorial intrusion in their community. However, neural activity in both hippocampus and lateral septum of subordinates increased when the intruder failed to establish dominance. Our results demonstrate how a social challenge results in multi-faceted behavioral, hormonal, and neural changes, depending on social status, sex, and the outcome of an intruder challenge. Taken together, our work provides novel insights into the mechanisms through which individual group members display context- and status-appropriate challenge responses in dynamic social groups.
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Similar contradictions were reported for septal lesion studies. In rats and in mice, septal damage decreased attack behaviours towards intruders and intraspecific fighting [121–123]. However, other classical mammalian studies reported the so called ‘septal rage’ behaviour, which is induced by septal damage and is typically associated with hyperactivity and a strong increase in aggressiveness [22].
Domestic chickens are able to distinguish familiar from unfamiliar conspecifics, however the neuronal mechanisms mediating this behaviour are almost unknown. Moreover, the lateralisation of chicks’ social recognition has only been investigated at the behavioural level, but not at the neural level. The aim of the present study was to test the hypothesis that exposure to unfamiliar conspecifics will selectively activate septum, hippocampus or nucleus taeniae of the amygdala of young domestic chicks. Moreover we also wanted to test the lateralisation of this response. For this purpose, we used the immediate early gene product c-Fos to map neural activity. Chicks were housed in pairs for one week. At test, either one of the two chicks was exchanged by an unfamiliar individual (experimental ‘unfamiliar’ group) or the familiar individual was briefly removed and then placed back in its original cage (control ‘familiar’ group). Analyses of chicks’ interactions with the familiar/unfamiliar social companion revealed a higher number of social pecks directed towards unfamiliar individuals, compared to familiar controls. Moreover, in the group exposed to the unfamiliar individual a significantly higher activation was present in the dorsal and ventral septum of the left hemisphere and in the ventral hippocampus of the right hemisphere, compared to the control condition. These effects were neither present in other subareas of hippocampus or septum, nor in the nucleus taeniae of the amygdala. Our study thus indicates selective lateralised involvement of domestic chicks’ septal and hippocampal subregions in responses to unfamiliar conspecific.
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The lateral septum represents one of the nodes of the social behaviour network [191] and is also connected to the mesolimbic reward system, making it a key element in a larger social decision making network [205]. Indeed, many studies in mammals and in birds have implicated the lateral septum in a variety of social behaviours, such as social memory, communication, gregariousness, individual recognition, dominance hierarchies, territoriality, aggression, sexual behaviour, pair-bonding, parental and anxiety-related behaviours, which are mainly mediated through neuropeptide signalling based on vasopressin and oxytocin receptors (or its avian homologous vasotocin and mesotocin) [199,202,206,207–237]. We found that simple exposure of visually naïve animals to an alive, behaving conspecific selectively activated septal areas, showing their involvement in recognition of animate creatures directly after birth [238,274].
To what extent are filial responses the outcome of spontaneous or acquired preferences? The case of domestic chicks illustrates the connection between predisposed and learned knowledge in early social responses. In the absence of specific experience, chicks prefer to approach objects that are more similar to natural social partners (e.g. they prefer face-like configurations, biological motion, self-propelled objects and those that move at variable speed). Spontaneous preferences are complemented by filial imprinting, a powerful learning mechanism that enables chicks to quickly learn the features of specific social partners. While neurobiological studies have clarified that the substrates of spontaneous and learned preferences are at least partially distinct in chicks, evidence shows that spontaneous preferences might orient and facilitate imprinting on animate stimuli, such as the mother hen, and that hormones facilitate and strengthen preferences for predisposed stimuli. Preferences towards animate stimuli are observed in human neonates as well. The remarkable consistency between the perceptual cues attended to by newborn babies and naïve chicks suggests that the attentional biases observed in babies are unlikely to result from very rapid post-natal learning, and confirms that research on precocial species can inform and guide human infant research with regards to both typical and atypical development. This has potentially important biomedical implications, opening new possibilities for the early detection of subjects at risk for autism spectrum disorders. We show how the parallel investigation of predispositions in naïve chicks and human infants, both benefiting from contact with social partners since the beginning of life, has greatly improved our understanding of early responses to social stimuli at the behavioural and neurobiological level.
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This activity is organized around competing for access to the nape of a partner’s nape of the neck (Fig. 2), which is rubbed with the snout if contacted (Pellis and Pellis, 1987; Siviy and Panksepp, 1987). In serious fighting, bites are directed at the rump and lower dorsum (Blanchard et al., 1977). Thus, even though the tactics of attack and defense used during play fighting are superficially similar to those used during serious fighting, it is readily distinguished from serious fighting by the target of attack (Pellis and Pellis, 1987).
Negative social experiences during adolescence are central features for several stress-related mental illnesses. Social play fighting behavior in rats peaks during early adolescence and is essential for the final maturation of brain and behavior. Manipulation of the rat adolescent social experience alters many neurobehavioral measurements implicated in anxiety, depression, and substance abuse. In this review, we will highlight the importance of social play and the use of three separate social stress models (isolation-rearing, social defeat, and social instability stress) to disrupt the acquisition of this adaptive behavior. Social stress during adolescence leads to the development of anxiety and depressive behavior as well as escalated drug use in adulthood. Furthermore, sex- and age-dependent effects on the hormonal stress response following adolescent social stress are also observed. Finally, manipulation of the social experience during adolescence alters stress-related neural circuits and monoaminergic systems. Overall, positive social experiences among age-matched conspecifics during rat adolescence are critical for healthy neurobehavioral maturation.
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Numerous animal species display behavioral changes in response to changes in social status or territory possession. For example, in male European starlings only males that acquire nesting sites display high rates of sexual and agonistic behavior. Past studies show that mu and delta opioid receptors regulate behaviors associated with social ascension or defeat. Opioids also act at kappa receptors, with dynorphin binding with the highest affinity; however, the role of these opioids in social behavior has not been well studied. We observed flocks of male starlings during the breeding season and ran quantitative real-time polymerase chain reaction (qPCR) to measure expression of kappa opioid receptors (OPRK1) and prodynorphin (PDYN) in brain regions involved in social behavior and motivation (ventral tegmental area [VTA], medial preoptic nucleus [mPOA]) and vocal behavior (Area X). Males with nesting territories displayed more sexual/agonistic behavior than males without nesting territories. They also had lower OPRK1 expression in VTA and mPOA. OPRK1 expression in VTA correlated negatively with sexual/agonistic behaviors, consistent with past studies showing kappa receptors in VTA to inhibit sociosexual behaviors. PDYN in mPOA correlated negatively with a measure of nesting behavior that may also reflect sexual motivation. PDYN in Area X related positively to song. Distinct patterns of OPRK1 and PDYN expression in VTA, mPOA, and Area X related to gonad volume, suggesting that breeding condition may modify (or be modified by) OPRK1 and PDYN expression. Studies are now needed to further characterize the role of OPRK1 and PDYN in status-appropriate social behaviors.
First exposure to an alive conspecific activates septal and amygdaloid nuclei in visually-naïve domestic chicks (Gallus gallus)
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Citation Excerpt :
Septum receives inputs from further social brain regions, such as the bed nucleus of stria terminalis (BNST), the medial amygdala [7–9] and dopaminergic projections from the ventral tegmental area (VTA) [10]. Many studies in mammals have implicated the lateral septum in a variety of social behaviors, such as social memory, individual recognition, dominance hierarchies, territoriality, aggression, sexual behavior, pair-bond, parental and anxiety-related behaviors, which are mainly mediate through neuropeptide signaling based on vasopressin and oxytocin receptors [11–29]. Similar to the mammalian septum, its avian homolog is located medial to the lateral ventricles and it also shares the connectivity profile of the mammalian septum, with massive inputs from the hippocampus and projections to the hypothalamus and midbrain [30–34].
The septal nuclei are an evolutionarily well-conserved part of the limbic system, present in all vertebrate groups. Functionally, septal nuclei are involved in many important aspects of social behavior and lateral septum is considered a node of the social decision making network, together with amygdaloid nuclei. Given the importance of septal nuclei for social behaviors, it is somewhat surprising that it has never been investigated whether they are involved in early social responses of naïve animals. In the present study we wanted to know if simple exposure of visually naïve newly hatched chicks to a visual object (an alive, behaving conspecific), that also contains all features to which chicks are known to express early social predispositions, will selectively activate septal areas. We measured brain activity by visualizing the immediate early gene product c-Fos with a standard immunohistochemical procedure. Notably, after a brief visual exposure to an alive behaving conspecific septum showed higher activation in experimental subjects, compared to baseline animals that were exposed to the same environment in the absence of the conspecific. This is, to the best of our knowledge, the first demonstration of septal involvement in early social responses. We also found similar effects in the nucleus taeniae and arcopallium (amygdala homologues), but not in the medial striatum. This result indicates that at least some nuclei of the social decision making network may participate in early responses to social stimuli. Future studies could capitalize on these results, by identifying the specific visual cues eliciting this effect.

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Brief reportSeptal lesions and aggressive behavior

Long-term effects of septal lesions and social experience on shock-elicited fighting in rats

J. Comp. Physiol. Psychol.

Limbic lesions and reflexive fighting

J. Comp. Physiol. Psychol.

Conspecific aggression in the laboratory rat

J. Comp. Physiol. Psychol.

Subcortical mechanisms in emotional behavior: Affective changes following septal forebrain lesions in the albino rat

J. of Comp. Physiol. Psychol.

Brief report
Septal lesions and aggressive behavior