Infant rats can learn time intervals before the maturation of the striatum: evidence from odor fear conditioning

Boulanger-Bertolus, Julie; Hegoburu, Chloé; Ahers, Jessica L.; Londen, Elizabeth; Rousselot, Juliette; Szyba, Karina; Thévenet, M; Sullivan-Wilson, T. A.; Doyère, Valérie; Sullivan, Regina M.; Mouly, Anne-Marie

doi:10.3389/fnbeh.2014.00176

Cited by 26 publications

(36 citation statements)

References 73 publications

(97 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Recently, second‐by‐second analyses of breathing and freezing have demonstrated temporally regulated behavior in rats as young as PN12 in an olfactory aversive conditioning, although the temporal pattern was not similar to the one observed in adults (Boulanger Bertolus et al ). Decreases in freezing and in respiratory rate were observed in anticipation to the US arrival in pups, whereas only the change in respiration was temporally related in adults.…”

Section: Ontogeny Of Interval Timingmentioning

confidence: 94%

Developmental emergence of fear/threat learning: neurobiology, associations and timing

Tallot

Doyère

Sullivan

2015

Genes Brain and Behavior

View full text Add to dashboard Cite

Pavlovian fear or threat conditioning, where a neutral stimulus takes on aversive properties through pairing with an aversive stimulus, has been an important tool for exploring the neurobiology of learning. In the past decades, this neurobehavioral approach has been expanded to include the developing infant. Indeed, protracted postnatal brain development permits the exploration of how incorporating the amygdala, prefrontal cortex and hippocampus into this learning system impacts the acquisition and expression of aversive conditioning. Here, we review the developmental trajectory of these key brain areas involved in aversive conditioning and relate it to pups’ transition to independence through weaning. Overall, the data suggests that adult-like features of threat learning emerge as the relevant brain areas become incorporated into this learning. Specifically, the developmental emergence of the amygdala permits cue learning and the emergence of the hippocampus permits context learning. We also describe unique features of learning in early life that block threat learning and enhance interaction with the mother or exploration of the environment. Finally, we describe the development of a sense of time within this learning and its involvement in creating associations. Together these data suggest that the development of threat learning is a useful tool for dissecting adult-like functioning of brain circuits, as well as providing unique insights into ecologically relevant developmental changes.

show abstract

Section: Ontogeny Of Interval Timingmentioning

confidence: 94%

Developmental emergence of fear/threat learning: neurobiology, associations and timing

Tallot

Doyère

Sullivan

2015

Genes Brain and Behavior

View full text Add to dashboard Cite

show abstract

“…Brains were sectioned in a cryostat (20 μm) at −20°C. Every third section was collected on a cover slip and exposed for 5 days along with standards ( 14 C standards 10 × 0.02 mCi, American Radiolabeled Chemicals Inc., St Louis, MO) and exposed to X-ray film in a cassette (Kodak, Rochester, NY) (Boulanger Bertolus et al, 2014; Debiec & Sullivan, 2014; Plakke, Freeman, & Poremba, 2009; Sullivan & Wilson, 1995). …”

Section: Animals and Methodsmentioning

confidence: 99%

Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering

Aïn

Perry

Nuñez

et al. 2016

Social Neuroscience

Self Cite

View full text Add to dashboard Cite

Social support can attenuate the behavioral and stress hormone response to threat, a phenomenon called social buffering. The mother’s social buffering of the infant is one of the more robust examples; yet we understand little about the neurobiology. Using a rodent model, we explore the neurobiology of social buffering by assessing neural processing of the maternal odor, a major cue controlling social buffering in rat pups. We used pups before (postnatal day (PN) 7) and after (PN14, PN23) the functional emergence of social buffering. Pups were injected with 14C 2-deoxyglucose (2-DG) and presented with the maternal odor, a control preferred odor incapable of social buffering (acetophenone), or no odor. Brains were removed, processed for autoradiography and brain areas identified as important in adult social buffering were assessed, including the amygdala basolateral complex (Basolateral Amygdala [BLA]), medial prefrontal cortex (mPFC), and anterior cingulate cortex (ACC). Results suggest dramatic changes in the processing of maternal odor. PN7 pups show mPFC and ACC activation, although PN14 pups showed no activation of the mPFC, ACC, or BLA. All brain areas assessed were recruited by PN23. Additional analysis suggests substantial changes in functional connectivity across development. Together, these results imply complex nonlinear transitions in the neurobiology of social buffering in early life that may provide insight into the changing role of the mother in supporting social buffering.

show abstract

“…In adults, beside the amygdala and piriform cortex, numerous other structures have been shown to exhibit changes following olfactory fear conditioning, from the earliest stages of olfactory processing (i.e., the olfactory receptors) (Jones et al 2008;Kass et al 2013), to associative cortices such as the entorhinal and perirhinal cortices (Herzog and Otto 1997;Funk and Amir 2000;Otto et al 2000;Jones et al 2007), but also structures such as the basal ganglia (Boulanger Bertolus et al 2014) and medial prefrontal cortex (Funk and Amir 2000;Kim and Richardson 2010;Sotres-Bayon and Quirk 2010). The hippocampus and the prefrontal cortex (PFC) have also been involved in olfactory fear conditioning, although not in the learning of the odor-shock association per se.…”

Section: Emergence Of Amygdala-dependent Fear Learningmentioning

confidence: 99%

“…Interestingly, high temporal resolution analysis of the respiratory rate during the fearful conditioned stimulus presentation revealed the emergence of a temporal pattern linked to the duration of the interval between the onset of the CS and the arrival of the US, suggesting that the animals readily learn the temporal relationships between the two events (Shionoya et al 2013). Importantly in pups, the respiratory response is also modulated by the duration of CS-US interval, allowing to assert that pups as young as PN12 are able to encode time (Boulanger Bertolus et al 2014). …”

mentioning

confidence: 99%

See 1 more Smart Citation

Ecologically relevant neurobehavioral assessment of the development of threat learning

2016

Self Cite

View full text Add to dashboard Cite

As altricial infants gradually transition to adults, their proximate environment changes. In three short weeks, pups transition from a small world with the caregiver and siblings to a complex milieu rich in dangers as their environment expands. Such contrasting environments require different learning abilities and lead to distinct responses throughout development. Here, we will review some of the learned fear conditioned responses to threats in rats during their ontogeny, including behavioral and physiological measures that permit the assessment of learning and its supporting neurobiology from infancy through adulthood. In adulthood, odor-shock conditioning produces robust fear learning to the odor that depends upon the amygdala and related circuitry. Paradoxically, this conditioning in young pups fails to support fear learning and supports approach learning to the odor previously paired with shock. This approach learning is mediated by the infant attachment network that does not include the amygdala. During the age range when pups transition from the infant to the adult circuit (10 -15 d old), pups have access to both networks: odor -shock conditioning in maternal presence uses the attachment circuit but the adult amygdala-dependent circuit when alone. However, throughout development (as young as 5 d old) the attachment associated learning can be overridden and amygdala-dependent fear learning supported, if the mother expresses fear in the presence of the pup. This social modulation of the fear permits the expression of defense reactions in life threatening situations informed by the caregiver but prevents the learning of the caregiver itself as a threat.

show abstract

Infant rats can learn time intervals before the maturation of the striatum: evidence from odor fear conditioning

Cited by 26 publications

References 73 publications

Developmental emergence of fear/threat learning: neurobiology, associations and timing

Developmental emergence of fear/threat learning: neurobiology, associations and timing

Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering

Ecologically relevant neurobehavioral assessment of the development of threat learning

Contact Info

Product

Resources

About