Lesions to Caudomedial Nidopallium Impair Individual Vocal Recognition in the Zebra Finch

Abstract

Many social animals can recognize other individuals by their vocalizations. This requires a memory system capable of mapping incoming acoustic signals to one out of many known individuals. Using the zebra finch, a social songbird that uses songs and distance calls to communicate individual identity (Elie & Theunissen, 2018), we tested the role of two cortical-like brain regions in a vocal recognition task. We found that the rostral region of the caudomedial nidopallium (NCM), a secondary auditory region of the avian pallium, was necessary for maintaining auditory memories for conspecific vocalizations in both male and female birds, while HVC, a premotor area that gates auditory input into the vocal motor and song learning pathways in male birds (Roberts & Mooney, 2013), was not. Both NCM and HVC have previously been implicated for processing the tutor song in the context of song learning (Sakata and Yazaki-Sugiyama, 2020). Our results suggest that NCM might not only store songs as templates for future vocal imitation but also songs and calls for perceptual discrimination of vocalizers in both male and female birds. NCM could therefore operate as a site for auditory memories for vocalizations used in various facets of communication. We also observed that new auditory memories could be acquired without intact HVC or NCM but that, for these new memories, NCM lesions caused deficits in either memory capacity or auditory discrimination. These results suggest that the high-capacity memory functions of the avian pallial auditory system depend on NCM.SIGNIFICANCE STATEMENT:Many aspects of vocal communication require the formation of auditory memories. Voice recognition, for example, requires a memory for vocalizers’ identifying acoustical features. In both birds and primates, the locus and neural correlates of these high-level memories remain poorly described. Previous work suggests that this memory formation is mediated by high-level sensory areas, not traditional memory areas such as the hippocampus. Using lesion experiments, we show that one secondary auditory brain region in songbirds that had previously been implicated in storing song memories for vocal imitation is also implicated in storing vocal memories for individual recognition. The role of the neural circuits in this region in interpreting the meaning of communication calls should be investigated in the future.

Tutor auditory memory for guiding sensorimotor learning in birdsong

“…In both sexes, NCM has been suggested to be the site of memory storage of auditory experiences, not exclusively for song learning. NCM lesions after conditioning with song stimulation diminishes song discrimination ability in adult males ( Gobes and Bolhuis, 2007 ; Canopoli et al, 2014 ; Yu et al, 2023 ), while lesions in adult females disrupt song preference to experienced songs ( Tomaszycki and Blaine, 2014 ).…”