Response to Wingfield's commentary on “A continuing saga: The role of testosterone in aggression”

Marler, Catherine A.; Oyegbile, Temitayo O.; Plavicki, Jessica; Trainor, Brian C.

doi:10.1016/j.yhbeh.2005.05.010

Cited by 38 publications

(29 citation statements)

References 16 publications

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“…The post-victory surge in plasma testosterone peaked 15-min after the encounter. This testosterone surge is quicker than in guinea pigs and California mice, where 45–min is the ideal interval to capture a post-victory rise in testosterone (Marler et al, 2005; Sachser and Pröve, 1984). However, our findings are consistent with Siberian hamsters, where plasma testosterone increases immediately after winning an aggressive encounter (Scotti et al, 2009).…”

Section: Discussionmentioning

confidence: 93%

Winning agonistic encounters increases testosterone and androgen receptor expression in Syrian hamsters

Clinard

Barnes

Adler

et al. 2016

Hormones and Behavior

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Winning aggressive disputes is one of several experiences that can alter responses to future stressful events. We have previously tested dominant and subordinate male Syrian hamsters in a conditioned defeat model and found that dominant individuals show less change in behavior following social defeat stress compared to subordinates and controls, indicating a reduced conditioned defeat response. Resistance to the effects of social defeat in dominants is experience-dependent and requires the maintenance of dominance relationships for 14 days. For this study we investigated whether winning aggressive interactions increases plasma testosterone and whether repeatedly winning increases androgen receptor expression. First, male hamsters were paired in daily 10-min aggressive encounters and blood samples were collected immediately before and 15-min and 30-min after the formation of dominance relationships. Dominants showed an increase in plasma testosterone at 15-min post-interaction compared to their pre-interaction baseline, whereas subordinates and controls showed no change in plasma testosterone. Secondly, we investigated whether 14 days of dominant social status increased androgen or estrogen alpha-receptor immunoreactivity in brain regions that regulate the conditioned defeat response. Dominants showed more androgen, but not estrogen alpha, receptor immuno-positive cells in the dorsal medial amygdala (dMeA) and ventral lateral septum (vLS) compared to subordinates and controls. Finally, we showed that one day of dominant social status was insufficient to increase androgen receptor immunoreactivity compared to subordinates. These results suggest that elevated testosterone signaling at androgen receptors in the dMeA and vLS might contribute to the reduced conditioned defeat response exhibited by dominant hamsters.

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Section: Discussionmentioning

confidence: 93%

Winning agonistic encounters increases testosterone and androgen receptor expression in Syrian hamsters

Clinard

Barnes

Adler

et al. 2016

Hormones and Behavior

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show abstract

“…The T pulse that occurs after either male-male antagonistic encounters or malefemale sexual encounters may induce males to differentially allocate time based on location of the encounter [7]. Aggressive encounters can induce CPPs per se [42,43], and the T pulses following a fight might mediate the CPPs for the location in which a given encounter occurs [44]. Therefore, the T-induced CPPs might influence territoriality by adjusting site preferences during instances of territory settlement.…”

Section: Resultsmentioning

confidence: 99%

Pair bonding prevents reinforcing effects of testosterone in male California mice in an unfamiliar environment

Zhao

Marler

2014

Proc. R. Soc. B.

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Testosterone (T) can be released by stimuli such as social interactions, and thereby influence future social behaviours. Because the reinforcing effects of T can induce preferences for specific environmental locations, T has the potential to alter behaviour through space use. In a monogamous species, this T pulse may contribute differently to space use in sexually naive (SN) and pair-bonded (PB) males: SN males may be more likely to explore new areas to set up a territory than PB males, which are more likely to defend an existing, established territory. In this study, we test for variation in T-driven space use by examining variation in the formation of conditioned place preferences (CPPs) in SN and PB male California mice. In the threechambered CPP apparatus, subcutaneous administrations of physiological levels of T were used to repeatedly condition SN and PB males to a side chamber, which is an unfamiliar/neutral environment. The final tests revealed that T-induced CPPs in the side chamber are developed in SN, but not PB males. This study fills a gap in our knowledge about plasticity in the rewarding nature of T pulses, based on past social experience.

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“…This complex pattern includes fluctuations in response to changing social conditions. Here, we artificially induce three individual transient increases via injections that mimic natural changes in T found in intact California mice both after winning a male–male encounter (Fuxjager et al, ; Marler et al, ; Oyegbile & Marler, ) and also after male–female encounters (X Zhao & CA Marler, unpublished).…”

Section: Discussionmentioning

confidence: 99%

“…There has been uncertainty as to how these individual transient increases in T (as compared to long‐term changes via implants) can influence behavior (Gleason et al, ; Marler, Oyegbile, Plavicki, & Trainor, ). For example, male California mice produce an increase in T over baseline levels 45 min after both male–male encounters (Marler et al, ) and male–female encounters (X Zhao & CA Marler unpublished data). Transient increases in T likely occur in California mice in natural settings in the field, as elegantly described by Wingfield and others for avian species (Wingfield et al, ).…”

Section: Introductionmentioning

confidence: 99%

Testosterone pulses at the nest site modify ultrasonic vocalization types in a monogamous and territorial mouse

2018

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Modulation of baseline testosterone (T) via long‐lasting T implants alters territorial, sexual, and social behavior of animals in the field. Transient T increases occur in numerous species after social interactions, but these transient increases in T have not been manipulated in the field. In the laboratory, these T increases can influence future behavior for days, causing changes in social behavior and inducing preferences for specific locations. We manipulated transient increases in T in the field at the nests of the monogamous and territorial California mouse (Peromyscus californicus) to examine long‐term (>24 hr) changes in ultrasonic vocalizations (USVs). Males of bonded male–female dyads (=pair) were administered a T injection (vs. saline) three times over seven days and USVs of the male–female dyad were measured for three days after the last injection. At T nests, the male–female dyad produced significantly more 1SV (one call SV: an SV is a sustained vocalization that is long in duration and low in modulation) and 4SV (four call SV) type USVs than controls, but no significant changes in aggressive barks. Overall, male–female dyad mice at T nests produced a greater diversity in call types such that 1SV, 4SV, 5SV, and a complex sweep were produced at T nests but not control nests. There were significantly more USVs produced at T nests on night 2 after the final injection. There were no differences in spectral characteristics of SV calls or aggressive barks between T and control nests. The function of the changes that occurred is unknown, but is consistent with increased long‐term changes in behavioral interactions with nest mates and may reflect T‐induced conditioned place preferences to the nest site. Significantly, transient increases in T influence future acoustic communication under field conditions with competing biotic and abiotic stimuli.

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Response to Wingfield's commentary on “A continuing saga: The role of testosterone in aggression”

Cited by 38 publications

References 16 publications

Winning agonistic encounters increases testosterone and androgen receptor expression in Syrian hamsters

Winning agonistic encounters increases testosterone and androgen receptor expression in Syrian hamsters

Pair bonding prevents reinforcing effects of testosterone in male California mice in an unfamiliar environment

Testosterone pulses at the nest site modify ultrasonic vocalization types in a monogamous and territorial mouse

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