Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

An intriguing phenomenon in the neurobiology of language is lateralization: the dominant role of one hemisphere in a particular function. Lateralization is not exclusive to language because lateral differences are observed in other sensory modalities, behaviors, and animal species. Despite much scientific attention, the function of lateralization, its possible dependence on experience, and the functional implications of such dependence have yet to be clearly determined. We have explored the role of early experience in the development of lateralized sensory processing in the brain, using the songbird model of vocal learning. By controlling exposure to natural vocalizations (through isolation, song tutoring, and muting), we manipulated the postnatal auditory environment of developing zebra finches, and then assessed effects on hemispheric specialization for communication sounds in adulthood. Using bilateral multielectrode recordings from a forebrain auditory area known to selectively process species-specific vocalizations, we found that auditory responses to species-typical songs and long calls, in both male and female birds, were stronger in the right hemisphere than in the left, and that right-side responses adapted more rapidly to stimulus repetition. We describe specific instances, particularly in males, where these lateral differences show an influence of auditory experience with song and/or the bird's own voice during development.auditory | development | electrophysiology | lateralization | songbird

Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 92%

Hemispheric differences in processing of vocalizations depend on early experience

Phan

Vicario

2010

“…The current NMR technology with strong magnets (7T and 9T) now makes it possible to obtain spatial resolutions that are accurate enough to study a brain as small as that of the songbird (74). Even 3T magnets are sufficient to detect how early social and song-learning experience affects patterns of song-specific auditory responses (75). An example of this approach is a recent study that used brain imaging to test how vocal and auditory experience and social environment shape auditory responses (76).…”

Section: Combining Behavioral Studies Of Song Development With Neuralmentioning

confidence: 99%

Quantification of developmental birdsong learning from the subsyllabic scale to cultural evolution

Lipkind

Tchernichovski

2011

Self Cite

Quantitative analysis of behavior plays an important role in birdsong neuroethology, serving as a common denominator in studies spanning molecular to system-level investigation of sensory-motor conversion, developmental learning, and pattern generation in the brain. In this review, we describe the role of behavioral analysis in facilitating cross-level integration. Modern sound analysis approaches allow investigation of developmental song learning across multiple time scales. Combined with novel methods that allow experimental control of vocal changes, it is now possible to test hypotheses about mechanisms of vocal learning. Further, song analysis can be done at the population level across generations to track cultural evolution and multigenerational behavioral processes. Complementing the investigation of song development with noninvasive brain imaging technology makes it now possible to study behavioral dynamics at multiple levels side by side with developmental changes in brain connectivity and in auditory responses.B irdsong neuroethology is a small but diverse and influential subfield of neuroscience, studied in ∼100 laboratories, and covering a range of research areas spanning the molecular to the organismal levels of investigation. The quantification of singing behavior has been a common denominator across most of those studies. Over the past four decades, birdsong neuroethology has made tremendous gains by incorporating existing tools for representing and analyzing sound (1). The sonogram (Fig. 1A) (2-4) provides an excellent descriptive model of singing behavior, and over the past decade several analysis approaches were developed that allow automatic segmentation categorization and comparison of vocal sounds (5-9). In this review, we describe the role of behavioral analysis in the progress made in birdsong neuroethology research.The past 20 y or so have seen rapid progress in understanding the neural and molecular processes involved in song. However, this progress was preceded by a long tradition of quantifying singing behavior (10, 11). Birdsong is uniquely amenable and attractive for behavioral analysis for a number of reasons: adult song is a structured behavior, repeated with a high degree of stereotypy (Fig. 1A). This makes it relatively easy to detect and characterize song structure and components (e.g., notes, syllables, motifs, and phrases) to align song renditions to each other, to assess the degree of similarity between songs, and, ultimately, to relate singing behavior to neuronal events and thus elucidate underlying neural mechanisms. We start by reviewing the role of behavioral quantification in achieving integration across levels of investigation. We then present a short outline of sound analysis techniques currently used for the tracking of developmental song learning, and an experimental approach for hypothesis-driven investigation of song development. Finally, we present a generalization of behavioral analysis to the population and cross-generation levels, and propose some ideas about n...

“…But some type of animal research may entail the same semantic problems as human studies with speech. Thus, in the studies using species-specific vocalization in birds (24)(25)(26), mice (27,28), sea lions (29), and monkeys (30)(31)(32)(33)(34)(35), as a rule, a left-hemisphere advantage (25,(27)(28)(29)(30)(31)(32)34), and in few studies a right-hemisphere advantage (26,35), was found-but no asymmetry (24,29,33,35) or a right-hemisphere bias (32,34) when non-species-specific sounds were applied [for review of animal studies, see supporting information (SI) Table S1]. Therefore, some authors concluded that the laterality effect is related to the communicative valence of signals rather than to their acoustic characteristics (36).…”

mentioning

confidence: 99%

Global versus local processing of frequency-modulated tones in gerbils: An animal model of lateralized auditory cortex functions

Wetzel

Ohl

Scheich

2008

Hemispheric asymmetries of speech and music processing might arise from more basic specializations of left and right auditory cortex (AC). It is not clear, however, whether such asymmetries are unique to humans, i.e., consequences of speech and music, or whether comparable lateralized AC functions exist in nonhuman animals, as evolutionary precursors. Here, we investigated the cortical lateralization of perception of linearly frequency-modulated (FM) tones in gerbils, a rodent species with human-like lowfrequency hearing. Using a footshock-reinforced shuttle-box avoidance go/no-go procedure in a total of 178 gerbils, we found that (i) the discrimination of direction of continuous FM (rising versus falling sweeps, 250-ms duration) was impaired by right but not left AC lesions; (ii) the discrimination of direction of segmented FM (50-ms segments, 50-ms silent gaps, total duration 250 ms) was impaired by bilateral but not unilateral AC lesions; (iii) the discrimination of gap durations (10 -30 ms) in segmented FM was impaired by left but not right AC lesions. AC lesions before and after training resulted in similar effects. Together, these experiments suggest that right and left AC, even in rodents, use different strategies in analyzing FM stimuli. Thus, the right AC, by using global cues, determines the direction of continuous and segmented FM but cannot discriminate gap durations. The left AC, by using local cues, discriminates gap durations and determines FM direction only when additional segmental information is available.asymmetry ͉ lateralization ͉ rodents