Hemispheric asymmetry in new neurons in adulthood is associated with vocal learning and auditory memory.

Shuk C Tsoi,Carolyn L Pytte,Mimi L Phan,Utsav V Aiya,Kobi D Wasner,David S Vicario

doi:10.1371/journal.pone.0108929

Abstract

Many brain regions exhibit lateral differences in structure and function, and also incorporate new neurons in adulthood, thought to function in learning and in the formation of new memories. However, the contribution of new neurons to hemispheric differences in processing is unknown. The present study combines cellular, behavioral, and physiological methods to address whether 1) new neuron incorporation differs between the brain hemispheres, and 2) the degree to which hemispheric lateralization of new neurons correlates with behavioral and physiological measures of learning and memory. The songbird provides a model system for assessing the contribution of new neurons to hemispheric specialization because songbird brain areas for vocal processing are functionally lateralized and receive a continuous influx of new neurons in adulthood. In adult male zebra finches, we quantified new neurons in the caudomedial nidopallium (NCM), a forebrain area involved in discrimination and memory for the complex vocalizations of individual conspecifics. We assessed song learning and recorded neural responses to song in NCM. We found significantly more new neurons labeled in left than in right NCM; moreover, the degree of asymmetry in new neuron numbers was correlated with the quality of song learning and strength of neuronal memory for recently heard songs. In birds with experimentally impaired song quality, the hemispheric difference in new neurons was diminished. These results suggest that new neurons may contribute to an allocation of function between the hemispheres that underlies the learning and processing of complex signals.

Highlights

Converging evidence suggests that new neurons formed in adulthood contribute to the formation of new memories [1,2]
We first asked whether the numbers of new neurons in NCM differ between the hemispheres by injecting adult male zebra finches with bromodeoxyuridine (BrdU) 3x/day over a 3 day period to label new cells and sacrificing the birds 3162 days after the first BrdU injection to count new neurons co-labeled with antibodies to BrdU and the neuronal markers Hu or NeuN (Fig. 2B, as in [39])
There were no statistical differences in the Neuron Asymmetry Index between Hu+BrdU+ and NeuN+BrdU+ labeled cell counts; we combined the values for these cell groups for all analyses, except where specified

Summary

Introduction

Converging evidence suggests that new neurons formed in adulthood contribute to the formation of new memories [1,2]. One prominent example of cerebral lateralization is hemispheric dominance for the production and perception of language, but many other functions and brain regions show lateral differences in humans and animals [4,5,6,7,8,9,10], including regions that receive new neurons throughout adulthood [8,9,10,11,12,13]. The contribution of hemispheric asymmetry to sensorimotor learning can be assessed in this model because songbirds learn their communication signals by imitating a tutor, as humans do [16], and songbird brain areas that subserve motor and sensory aspects of song learning and production continuously receive new neurons throughout adulthood [17]. In a striking parallel with lateralized speech production and perception, songbird vocal processing areas are functionally lateralized, as demonstrated by behavioral, electrophysiological, fMRI, and immediate early gene studies [7,12,13,22,23,24,25,26,27,28,29,30]

Methods

Results

Conclusion