Parental state dynamically reshapes auditory processing of offspring vocalizations in zebra finches

Abstract

Parental care is critical for offspring survival. For many species, including humans, auditory cues unique to dependent offspring, such as baby cries, elicit the necessary behavior from parents to care for young. Despite this, we know little about how the brain encodes auditory cues specific to offspring. Zebra finches are an excellent model to study this. Zebra finches are biparental, meaning both male and female parents raise the young and rely on auditory cues (begging calls) to elicit chick feeding responses (parental behavior). Begging calls also become individually identifiable by the parents, necessitating higher-order learning/ association neural processes. It is well established that the caudomedial nidopallium (NCM), a higher-order region of secondary pallial cortex (analogous to the mammalian secondary auditory cortex), is involved in the perception of complex auditory signals in birds. It is unknown, however, if/how NCM responds to offspring begging calls. To begin testing this, we used high density silicon probes to record single-unit in vivo electrophysiology activity in the NCM of adult parenting and non-parenting zebra finches exposed to playbacks of their own chicks begging calls (parents only), novel age-matched begging calls (parents and non-parents), as well as novel adult male song and pure tone controls. Our results show that NCM neurons in parents respond more strongly (i.e., higher evoked firing rates) to both their own and novel chick begging calls and have higher baseline (spontaneous) firing rates in narrow spiking units relative to non-parents. Furthermore, NCM neurons in parenting females tend to show more selective responses towards their own chick begging calls, whereas those in males do not show similar levels of selectivity. These studies lay essential groundwork for future studies on how auditory responses can elicit parental behavior and how these responses may change over the chick-rearing period.