Social behaviors are crucial to all mammals. Although the prelimbic cortex (PL, part of medial prefrontal cortex) has been implicated in social behavior, it is not clear which neurons are relevant, nor how they contribute. We found that PL contains anatomically and molecularly distinct subpopulations that target 3 downstream regions that have been implicated in social behavior: the nucleus accumbens (NAc), amygdala, and ventral tegmental area. Activation of NAc-projecting PL neurons (PL-NAc), but not the other subpopulations, decreased preference for a social target. To determine what information PL-NAc neurons convey, we recorded selectively from them, and found that individual neurons were active during social investigation, but only in specific spatial locations. Spatially-specific manipulation of these neurons bidirectionally regulated the formation of a social-spatial association. Thus, the unexpected combination of social and spatial information within the PL-NAc may contribute to social behavior by supporting social-spatial learning.
SummaryPremotor circuits help generate complex behaviors, including those learned by imitation. Premotor circuits also can be activated during observation of another animal’s behavior, leading to speculation that they also participate in sensory learning important to imitation. Here we tested this idea by focally manipulating the brain activity of juvenile zebra finches, which learn to sing by memorizing and vocally copying the song of an adult tutor. Tutor song-contingent optogenetic or electrical disruption of neural activity in the pupil’s song premotor nucleus HVC prevented song copying, indicating that a premotor structure important to the temporal control of birdsong also helps encode the tutor song. In vivo multiphoton imaging and neural manipulations delineated a pathway and candidate synaptic mechanism through which tutor song information is encoded by premotor circuits. These findings provide evidence that premotor circuits help to encode sensory information about the behavioral model prior to shaping and executing imitative behaviors.
Summary Mutations of the FOXP2 gene impair speech and language development in humans and shRNA-mediated suppression of the avian orthologue FoxP2 disrupts song learning in juvenile zebra finches. How diminished FoxP2 levels affect vocal control and alter the function of neural circuits important to learned vocalizations remains unclear. Here we show that FoxP2 knockdown in the songbird striatum disrupts developmental and social modulation of song variability. Recordings in anaesthetized birds show that FoxP2 knockdown interferes with D1R-dependent modulation of activity propagation in a corticostriatal pathway important to song variability, an effect that may be partly attributable to reduced D1R and DARPP-32 protein levels. Furthermore, recordings in singing birds reveal that FoxP2 knockdown prevents social modulation of singing-related activity in this pathway. These findings show that reduced FoxP2 levels interfere with the dopaminergic modulation of vocal variability, which may impede song and speech development by disrupting reinforcement learning mechanisms.
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