Background A single episode of acute immobilization stress has previously been shown to trigger a delayed onset of anxiety-like behavior and spinogenesis in the basolateral amygdala (BLA) of rats. Spurred on by a seemingly paradoxical observation in which even a modest increase in corticosterone (CORT), caused by a single vehicle injection before stress, could dampen the delayed effects of stress, we hypothesized a protective role for glucocorticoids against stress. Methods We tested this hypothesis by analyzing how manipulations in CORT levels modulate delayed increase in anxiety-like behavior of rats on the elevated plus-maze 10 days after acute stress. We also investigated the cellular correlates of different levels of anxiety under different CORT conditions by quantifying spine density on Golgi-stained BLA principal neurons. Results CORT in drinking water for 12 hours preceding acute stress prevented delayed increase in anxiety rather than exacerbating it. Conversely, vehicle injection failed to prevent the anxiogenic effect of stress in bilaterally adrenalectomized rats. However, when CORT was restored in adrenalectomized rats by injection, the delayed anxiogenic effect of stress was once again blocked. Finally, high and low anxiety states were accompanied by high and low levels of BLA spine density. Conclusions Our findings suggest that the presence of elevated levels of CORT at the time of acute stress confers protection against the delayed enhancing effect of stress on BLA synaptic connectivity and anxiety-like behavior. These observations are consistent with clinical reports on the protective effects of glucocorticoids against the development of posttraumatic symptoms triggered by traumatic stress.

Controlled presentation of stimuli to anesthetized [1] or awake [2] animals suggested that neurons in sensory cortices respond to elementary features [3, 4], but we know little about neuronal responses evoked by social interactions. Here we investigate processing in the barrel cortex of rats engaging in social facial touch [5, 6]. Sensory stimulation by conspecifics differs from classic whisker stimuli such as deflections, contact poles [7, 8], or textures [9, 10]. A large fraction of barrel cortex neurons responded to facial touch. Social touch responses peaked when animals aligned their faces and contacted each other by multiple whiskers with small, irregular whisker movements. Object touch was associated with larger, more regular whisker movements, and object responses were weaker than social responses. Whisker trimming abolished responses. During social touch, neurons in males increased their firing on average by 44%, while neurons in females increased their firing by only 19%. In females, socially evoked and ongoing firing rates were more than 1.5-fold higher in nonestrus than in estrus. Barrel cortex represented socially different contacts by distinct firing rates, and the variation of activity with sex and sexual status could contribute to the generation of gender-specific neural constructs of conspecifics.

Social interactions involve multi-modal signaling. Here, we study interacting rats to investigate audio-haptic coordination and multisensory integration in the auditory cortex. We find that facial touch is associated with an increased rate of ultrasonic vocalizations, which are emitted at the whisking rate (∼8 Hz) and preferentially initiated in the retraction phase of whisking. In a small subset of auditory cortex regular-spiking neurons, we observed excitatory and heterogeneous responses to ultrasonic vocalizations. Most fast-spiking neurons showed a stronger response to calls. Interestingly, facial touch-induced inhibition in the primary auditory cortex and off-responses after termination of touch were twofold stronger than responses to vocalizations. Further, touch modulated the responsiveness of auditory cortex neurons to ultrasonic vocalizations. In summary, facial touch during social interactions involves precisely orchestrated calling-whisking patterns. While ultrasonic vocalizations elicited a rather weak population response from the regular spikers, the modulation of neuronal responses by facial touch was remarkably strong.DOI: http://dx.doi.org/10.7554/eLife.03185.001

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