Adult males buffer the cortisol response of young guinea pigs: Changes with age, mediation by behavior, and comparison with prefrontal activity

Hennessy, Michael B.; Watanasriyakul, W Tang; Price, Brittany C.; Bertke, Alexander; Schiml, Patricia A.

doi:10.1016/j.yhbeh.2017.12.017

Cited by 7 publications

(5 citation statements)

References 42 publications

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“…Electrode placement was explored in some animals by changing the depth of the electrode. Stimulation at a depth of approximately 5 mm from the cortical surface, most likely reflecting placement in prelimbic cortex ( Hennessy et al, 2018 ), yielded the largest and most consistent effects on MGN activity.…”

Section: Resultsmentioning

confidence: 99%

Hearing Loss Increases Inhibitory Effects of Prefrontal Cortex Stimulation on Sound Evoked Activity in Medial Geniculate Nucleus

Vis

Barry

Mulders

2022

Front. Synaptic Neurosci.

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Sensory gating is the process whereby irrelevant sensory stimuli are inhibited on their way to higher cortical areas, allowing for focus on salient information. Sensory gating circuitry includes the thalamus as well as several cortical regions including the prefrontal cortex (PFC). Defective sensory gating has been implicated in a range of neurological disorders, including tinnitus, a phantom auditory perception strongly associated with cochlear trauma. Recently, we have shown in rats that functional connectivity between PFC and auditory thalamus, i.e., the medial geniculate nucleus (MGN), changes following cochlear trauma, showing an increased inhibitory effect from PFC activation on the spontaneous firing rate of MGN neurons. In this study, we further investigated this phenomenon using a guinea pig model, in order to demonstrate the validity of our finding beyond a single species and extend data to include data on sound evoked responses. Effects of PFC electrical stimulation on spontaneous and sound-evoked activity of single neurons in MGN were recorded in anaesthetised guinea pigs with normal hearing or hearing loss 2 weeks after acoustic trauma. No effect, inhibition and excitation were observed following PFC stimulation. The proportions of these effects were not different in animals with normal hearing and hearing loss but the magnitude of effect was. Indeed, hearing loss significantly increased the magnitude of inhibition for sound evoked responses, but not for spontaneous activity. The findings support previous observations that PFC can modulate MGN activity and that functional changes occur within this pathway after cochlear trauma. These data suggest hearing loss can alter sensory gating which may be a contributing factor toward tinnitus development.

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Section: Resultsmentioning

confidence: 99%

Hearing Loss Increases Inhibitory Effects of Prefrontal Cortex Stimulation on Sound Evoked Activity in Medial Geniculate Nucleus

Vis

Barry

Mulders

2022

Front. Synaptic Neurosci.

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“…The similar social buffering effects on the behavioral level at PN18 and PN28 appear to be supported by different neural networks; the ventromedial (vm)PFC IL and PL subregions were only modulated by the mother in the PN28 animals. The PFC is a late-developing structure (Gee et al, 2013b; Schubert et al, 2015; Hennessy et al, 2018) and the older infant/child and adult literature validates the important role of the amygdala and vmPFC for social buffering in humans (Lungwitz et al, 2014; Hornstein et al, 2016; Hornstein and Eisenberger, 2017; van Rooij et al, 2017), nonhuman primates (Winslow et al, 2003; Suomi et al, 2008; Sanchez et al, 2015; Howell et al, 2017) and rodents (Hennessy et al, 2015; Penha Farias et al, 2019). The absence of a PFC effect in the youngest pups is consistent with the literature as well.…”

Section: Discussionmentioning

confidence: 99%

“…Social buffering wanes with maturation, although this effect can still be seen in adults of many species. While there appears to be some overlap in the neural mechanisms across development, the late-developing prefrontal cortex (PFC) appears critical in adult social buffering (Hennessy et al, 2006, 2015, 2018; Kiyokawa et al, 2007, 2012; Taylor et al, 2008; Upton and Sullivan, 2010; Inagaki and Eisenberger, 2012; Tottenham et al, 2012; Hostinar et al, 2015; Hornstein et al, 2016; Harrison et al, 2017; Hornstein and Eisenberger, 2017). Here, we focus on the PFC and its evolving role in social buffering of the threat response, targeting a developmental transition from dependence on the mother (postnatal day [PN] 18) to independence in preadolescent rats (PN28) weaned from the mother.…”

Section: Introductionmentioning

confidence: 99%

Infant Trauma Alters Social Buffering of Threat Learning: Emerging Role of Prefrontal Cortex in Preadolescence

Robinson-Drummer

Opendak

Blomkvist

et al. 2019

Front. Behav. Neurosci.

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Within the infant-caregiver attachment system, the primary caregiver holds potent reward value to the infant, exhibited by infants’ strong preference for approach responses and proximity-seeking towards the mother. A less well-understood feature of the attachment figure is the caregiver’s ability to reduce fear via social buffering, commonly associated with the notion of a “safe haven” in the developmental literature. Evidence suggests this infant system overlaps with the neural network supporting social buffering (attenuation) of fear in the adults of many species, a network known to involve the prefrontal cortex (PFC). Here, using odor-shock conditioning in young developing rats, we assessed when the infant system transitions to the adult-like PFC-dependent social buffering of threat system. Rat pups were odor-shock conditioned (0.55 mA–0.6 mA) at either postnatal day (PN18; dependent on mother) or 28 (newly independent, weaned at PN23). Within each age group, the mother was present or absent during conditioning, with PFC assessment following acquisition using 14 C 2-DG autoradiography and cue testing the following day. Since the human literature suggests poor attachment attenuates the mother’s ability to socially buffer the infants, half of the pups at each age were reared with an abusive mother from PN8–12. The results showed that for typical control rearing, the mother attenuated fear in both PN18 and PN28 pups, although the PFC [infralimbic (IL) and ventral prelimbic (vPL) cortices] was only engaged at PN28. Abuse rearing completely disrupted social buffering of pups by the mother at PN18. The results from PN28 pups showed that while the mother modulated learning in both control and abuse-reared pups, the behavioral and PFC effects were attenuated after maltreatment. Our data suggest that pups transition to the adult-like PFC social support circuit after independence from the mother (PN28), and this circuit remains functional after early-life trauma, although its effectiveness appears reduced. This is in sharp contrast to the effects of early life trauma during infancy, where social buffering of the infant is more robustly impacted. We suggest that the infant social buffering circuit is disengaged by early-life trauma, while the adolescent PFC-dependent social buffering circuit may use a safety signal with unreliable safety value.

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“…The presence of the mother, even when anesthetized, reduces pups' cortisol response during exposure to novelty [52] quite possibly again by inhibiting noradrenergic input [53]. In contrast, adult males reduce pups' cortisol response in a novel environment when the male is awake and actively engaging the pup, but not, unlike the case for the mother, when then male is anesthetized [54]. The active male increases excitation in the pup's PFC, which may activate known inhibitory connections to the PVN [55] (Figure 1, middle).…”

Section: Mechanism Of Social Buffering Of Hpa Responsesmentioning

confidence: 98%

Psychological Stress, Its Reduction, and Long-Term Consequences: What Studies with Laboratory Animals Might Teach Us about Life in the Dog Shelter

Hennessy

Willen²,

Schiml

2020

Animals

Self Cite

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There is a long history of laboratory studies of the physiological and behavioral effects of stress, its reduction, and the later psychological and behavioral consequences of unmitigated stress responses. Many of the stressors employed in these studies approximate the experience of dogs confined in an animal shelter. We review how the laboratory literature has guided our own work in describing the reactions of dogs to shelter housing and in helping formulate means of reducing their stress responses. Consistent with the social buffering literature in other species, human interaction has emerged as a key ingredient in moderating glucocorticoid stress responses of shelter dogs. We discuss variables that appear critical for effective use of human interaction procedures in the shelter as well as potential neural mechanisms underlying the glucocorticoid-reducing effect. We also describe recent studies in which enrichment centered on human interaction has been found to reduce aggressive responses in a temperament test used to determine suitability for adoption. Finally, we suggest that a critical aspect of the laboratory stress literature that has been underappreciated in studying shelter dogs is evidence for long-term behavioral consequences—often mediated by glucocorticoids—that may not become apparent until well after initial stress exposure.

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Adult males buffer the cortisol response of young guinea pigs: Changes with age, mediation by behavior, and comparison with prefrontal activity

Cited by 7 publications

References 42 publications

Hearing Loss Increases Inhibitory Effects of Prefrontal Cortex Stimulation on Sound Evoked Activity in Medial Geniculate Nucleus

Hearing Loss Increases Inhibitory Effects of Prefrontal Cortex Stimulation on Sound Evoked Activity in Medial Geniculate Nucleus

Infant Trauma Alters Social Buffering of Threat Learning: Emerging Role of Prefrontal Cortex in Preadolescence

Psychological Stress, Its Reduction, and Long-Term Consequences: What Studies with Laboratory Animals Might Teach Us about Life in the Dog Shelter

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