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We ask whether artificially induced testosterone pulses (T-pulses), administered to males in the wild at the territory boundary, adjust location preferences within the territory. Multiple transient T-pulses occurring after social interactions in males can alter behaviour and spatial preferences. We previously found that T-pulses administered at the nest induce male California mice, a biparental and territorial species, to spend more time at the nest likely through conditioned place preferences. We hypothesized that T’s reinforcing effects would increase future time by the T-injected males at the boundary and promote territorial defence. Contrary to predictions, T-pulses induced a decrease in male time at the boundary, and instead appeared to promote male territorial/home range expansion, accompanied by shorter sustained vocalizations (SVs) and decreased proportion of three SV bouts. Shorter SVs are associated with aggression in the laboratory. Furthermore, in response to T-male behavioural changes, uninjected female partners decreased boundary time. Our results suggest new functions for socially induced T-pulses, such as extending territorial boundaries/home ranges. Location preferences induced through reinforcing/rewarding mechanisms may be more plastic and dependent on physical and social contexts than previously thought. Moreover, the results suggest that location preferences produced through rewarding/reinforcing mechanisms can be viewed from adaptive perspectives to influence future behaviour. 

Central to the navigation of an ever-changing environment is the ability to form positive associations with places and conspecifics. The functions of location and social conditioned preferences are often studied independently, limiting our understanding of their interplay. Furthermore, a de-emphasis on natural functions of conditioned preferences has led to neurobiological interpretations separated from ecological context. By adopting a naturalistic and ethological perspective, we uncover complexities underlying the expression of conditioned preferences. Development of conditioned preferences is a combination of motivation, reward, associative learning, and context, including for social and spatial environments. Both social- and location-dependent reward-responsive behaviors and their conditioning rely on internal state-gating mechanisms that include neuroendocrine and hormone systems such as opioids, dopamine, testosterone, estradiol, and oxytocin. Such reinforced behavior emerges from mechanisms integrating past experience and current social and environmental conditions. Moreover, social context, environmental stimuli, and internal state gate and modulate motivation and learning via associative reward, shaping the conditioning process. We highlight research incorporating these concepts, focusing on the integration of social neuroendocrine mechanisms and behavioral conditioning. We explore three paradigms: 1) conditioned place preference, 2) conditioned social preference, and 3) social conditioned place preference. We highlight nonclassical species to emphasize the naturalistic applications of these conditioned preferences. To fully appreciate the complex integration of spatial and social information, future research must identify neural networks where endocrine systems exert influence on such behaviors. Such research promises to provide valuable insights into conditioned preferences within a broader naturalistic context. 

Changing social environments such as the birth of young or aggressive encounters present a need to adjust behavior. Previous research examined how long-term changes in steroid hormones mediate these adjustments. We tested the novel concept that the rewarding effects of transient testosterone pulses (T-pulses) in males after social encounters alter their spatial distribution on a territory. In free-living monogamous California mice ( Peromyscus californicus ), males administered three T-injections at the nest spent more time at the nest than males treated with placebo injections. This mimics T-induced place preferences in the laboratory. Female mates of T-treated males spent less time at the nest but the pair produced more vocalizations and call types than controls. Traditionally, transient T-changes were thought to have transient behavioral effects. Our work demonstrates that in the wild, when T-pulses occur in a salient context such as a territory, the behavioral effects last days after T-levels return to baseline.