Natural predator and a human stimulus differently affect the behavior, cortisol and cerebral hemisphere activity of marmoset monkeys

Abstract

The behavior, cortisol concentration and cerebral hemisphere activity of twelve marmoset monkeys were determined during standardized predatory stress-related events. Each subject was submitted to three 5-min trials, randomly held at 2-week intervals: a human intruder, a taxidermized oncilla cat and a no-stimulus control trial. Stimuli were positioned outside the home-cage and the ensuing reaction recorded. Baseline tympanic membrane temperature (TMT) was subtracted from the post-trial measure to determine changes in blood flow induced by ipsilateral brain activity. Cortisol was assayed immediately after the post-trial TMT assessments. Both genders reacted fearfully/anxiously towards the stimuli - each condition inducing a distinct pattern. Cortisol increased only when females were confronted with the wildcat, with higher levels of alarm calls predicting lower cortisol release. When either stimulus was present, changes in TMT were detected, albeit only in the right ear. The specific directional shift in temperature was gender- and stimulus-dependent, requiring further investigation. The control trial did not alter any of the parameters. Marmosets thus exhibit flexible multileveled coping strategies towards different aversive events, yet in general these seem to be asymmetrically processed by the right cerebral hemisphere.

Baseline cortisol levels and social behavior differ as a function of handedness in marmosets (Callithrix jacchus)

“…As noted above, Gordon and Rogers () measured reactivity of the monkeys in face of a novel task, while Braccini and Caine () measured responses to a fearful situation. Additional evidence that fearful situations induce right hemisphere activation in marmosets comes from a recent study using tympanic membrane temperature thermometry (Pereira, Duarte, Maior, & Barros, ). The authors found that changes in temperature after exposure to two types of threatening stimuli (human intruder or predator) were specific to the right ear (i.e, right hemisphere) in marmosets.…”

Time-Dependent Changes in Cortisol and Tympanic Temperature Lateralization During Food Deprivation Stress in Marmoset Monkeys

“…For example, TMT increased bilaterally after a brief restraint event ( bushbabies : Hanbury et al, 2011 ), whereas a right-side dominance was seen after longer intervals ( marmosets : Pereira et al, 2019 ) or recurring episodes ( marmosets : Tomaz et al, 2003 ). On the other hand, brief exposures to a predator model were asymmetrically processed by the right hemisphere ( marmosets : Hook-Costigan and Rogers, 1998 ; Souza Silva et al, 2007 ; Pereira et al, 2018 ), but the response to a food-retrieval task associated with a predatory stimulus was blunted by unilateral lesions on either side ( macaques : Izquierdo and Murray, 2004 ). When processing emotionally-laden stimuli, aspects other than event duration may contribute to the variability in functional hemisphere bias, or even lack thereof, including the type of stimulus (e.g., restraint vs. predatory stress), species (e.g., response to unfamiliar human by marmosets vs. macaques; Izquierdo and Murray, 2004 ; Pereira et al, 2018 ) and trait-like characteristics (e.g., fearful temperament; Kalin et al, 1998 ).…”

“…A dilution of 1:50 serum:diluent was used (Multi-diluent 3, Siemens, Brazil). CLIA and dilution parameters were based on a previous study in this species (Pereira et al, 2018 ). Assay sensitivity was 1 μg/dl, and inter- and intra-assay coefficient of variation from pooled serum were 9.8% and 7.5%, respectively.…”

“…It reflects ipsilateral shifts in cerebral blood flow caused by activity-induced changes in brain temperature (Baker et al, 1972 ; Schiffer et al, 1999 ; Schuman et al, 1999 ; Yablonskiy et al, 2000 ). We hypothesized that FD stress would alter the marmosets’ right TMT and hemisphere activity, yet did not predict the direction of the TMT shift, as this has been shown to increase and decrease in response to stress in this species (Pereira et al, 2018 , 2019 ).…”

“…For this, we delayed routine food placement for either 3 h or 6 h. Blood cortisol concentration was used as a hormonal measure of the stress response, while a change in tympanic membrane temperature (TMT) was used as an indicator of hemisphere activity. TMT can be a fast, inexpensive, non-invasive, and indirect index of real-time changes in hemisphere activity (Cherbuin and Brinkman, 2007 ; Propper and Brunyé, 2013 ), including that of marmosets (Tomaz et al, 2003 ; Pereira et al, 2018 , 2019 ). It reflects ipsilateral shifts in cerebral blood flow caused by activity-induced changes in brain temperature (Baker et al, 1972 ; Schiffer et al, 1999 ; Schuman et al, 1999 ; Yablonskiy et al, 2000 ).…”