Mirrored patterns of lateralized neuronal activation reflect old and new memories in the avian auditory cortex

Abstract

In monolingual humans, language-related brain activation shows a distinct lateralized pattern, in which the left hemisphere is often dominant. Studies are not as conclusive regarding the localization of the underlying neural substrate for language in sequential language learners. Lateralization of the neural substrate for first and second language depends on a number of factors including proficiency and early experience with each language. Similar to humans learning speech, songbirds learn their vocalizations from a conspecific tutor early in development. Here, we show mirrored patterns of lateralization in the avian analog of the mammalian auditory cortex (the caudomedial nidopallium [NCM]) in sequentially tutored zebra finches, in response to their first tutor song, learned early in development, and to their second tutor song, learned later in development. The greater the retention of song from their first tutor, the more right-dominant the birds were when exposed to that song; the more birds learned from their second tutor, the more left-dominant they were when exposed to that song. Thus, the avian auditory cortex may preserve lateralized neuronal traces of old and new tutor song memories, which are dependent on proficiency of song learning. There is striking resemblance in humans: early-formed language representations are maintained in the brain even if exposure to that language is discontinued. The switching of hemispheric dominance related to the acquisition of early auditory memories and subsequent encoding of more recent memories may be an evolutionary adaptation in vocal learners necessary for the behavioral flexibility to acquire novel vocalizations, such as a second language.

Audition and Hemispheric Specialization in Songbirds and New Evidence from Australian Magpies

“…We already know from studies of song learning in zebra finches that new songs learned are memorized in the right hemisphere while the original song (long-term memory) is retrieved from and shows neural activity in the left hemisphere [27]. However, according to the results reported by Olsen et al [97], direction and strength of laterality depend on how well each song is learned and by whom: The greater the retention of song from their first tutor, the more right-dominant the birds were when exposed to that song; but the more birds learned from their second tutor, the more left-dominant they were when exposed to the first song [97]. Lateralized memory strengthens the performance of well-learned song and presumably enables the bird to be competitive for females in the coming season.…”

Lateral Asymmetry of Brain and Behaviour in the Zebra Finch, Taeniopygia guttata

“…Furthermore, male zebra finches learn their song from other birds, by imitating the song of a tutor heard during a sensitive period of development [2,3]. These and other aspects of zebra finch song have been studied in considerable detail and compared to speech in humans [4][5][6][7].…”

“…However, measuring expression of the immediate early gene ZENK in zebra finches exposed to the auditory and/or visual aspects of courtship, Avery et al [17] found left hemispheric dominance (i.e., hearing courtship song and seeing dancing by the courting male causes more neural activity in the left than the right hemisphere). Recent studies have demonstrated that both hemispheres attend to song but to different aspects of it [1], and that the direction of asymmetry depends on whether the memory of song is old or new [6].…”

“…Demonstrating that the direction of lateralisation depends on learning and memory, Moorman et al [18] reported left-sided dominance of ZENK expression in the higher vocal centre of juvenile males exposed to their tutor's song but not in those exposed to unfamiliar song. Olson et al [6] found that the direction of laterality of song memory depends on strength of learning; the more the zebra finches learnt and remembered the song of their first tutor, the more right lateralised they were, as assessed by ZENK expression. By contrast, the more they learnt from a second tutor, the more left-lateralised they were.…”

Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

“…Interestingly, some evidence suggests that NCM may be functionally left lateralized for tutor song sensory learning (Chirathivat, Raja, & Gobes, 2015;Moorman et al, 2012;Moorman & Nicol, 2015;Olson, Maeda, & Gobes, 2016;cf. Phan & Vicario, 2010;Voss et al, 2007).…”