Vocalization–whisking coordination and multisensory integration of social signals in rat auditory cortex

Abstract

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

Barrel Cortex Membrane Potential Dynamics in Social Touch

“…We find that while calling rates of our headfixed animals were low, stimulus animals called at higher rates similar to interacting animals (data not shown; Rao et al, 2014). Hence, ultrasonic vocalizations could also contribute to the pre-contact effects seen in our interactions.…”

Subject sex and partner sex modulate social touch responses across multiple cortical areas

“…In social facial touch, rats align their snouts and whisk to palpate each other's face with their mystacial vibrissae. We recorded the behavior of male and female rats by videography from above in visual darkness under infrared illumination 28,32,33 . (B) Anatomical location of vibrissa motor cortex ('VMC' -the primary motor representation of the mystacial vibrissae), cingulate cortex ('ACC' -a putative homolog of human/primate anterior cingulate cortex), prelimbic cortex ('PrL' -a putative homolog of human/primate medial prefrontal cortex), barrel cortex ('S1' -the primary somatosensory representation of the mystacial vibrissae) and auditory cortex ('A1').…”

“…A portion of the data analyzed here has been presented in previous studies where we investigated other questions (ref. 28,32,33 , see Methods).…”

“…The rat behavior was recorded at low video speed from above with a 25 Hz or 30 Hz digital camera, synchronized to the electrophysiological data acquisition using TTL pulses. Typically, recording sessions were performed in four to eight 10-15 min blocks, where we would present either one or two conspecifics (of both sexes) in each block, randomly, see 28,32,33 . Video frames were labeled blind to the spike data.…”

“…The auditory cortex data, recorded throughout all cortical layers, has previously been published in ref. 32 . The recordings from deep layers of vibrissa motor cortex has previously been presented in ref.…”