Pattern of Interhemispheric Synchronization in HVc During Singing Correlates With Key Transitions in the Song Pattern

Abstract

Many complex voluntary behaviors require that motor commands be tightly coordinated between cerebral hemispheres. The neural mechanisms underlying such coordination, however, remain poorly understood. Song production in birds is a highly stereotyped learned motor behavior that requires finely tuned coordination between hemispheres. In the present study, neural activity was recorded simultaneously from the song control nucleus HVc in each hemisphere of singing adult male zebra finches ( Taeniopygia guttata). In all cases, the pattern of recorded multiunit activity in each hemisphere was highly correlated during short segments of the song motor pattern. These correlated segments often consisted of multiple short bursts of activity. Because of the absence of interhemispheric connections between song control nuclei, these observations suggest that HVc activity is “synchronized” by common inputs to both hemispheres. Using sliding-window cross-covariance analyses, periods of high interhemispheric synchronization were found to be time-locked to the acoustic onset of syllables and notes. In some cases, precisely synchronized bursts in both hemispheres were also observed during periods associated with the intersyllable silent interval. In all cases, activity was correlated between hemispheres independently of the recording site, suggesting that all regions of HVc may be globally synchronized during these short segments of the song. Given the anatomical organization of the song system, inputs originating from either thalamus or midbrain are proposed to act as timing signals that initiate and synchronize intrinsic motor networks within each HVc thus allowing for the precise coordination of motor commands across hemispheres.

Brainstem and Forebrain Contributions to the Generation of Learned Motor Behaviors for Song

“…In the avian song system, for example, forebrain song control nuclei HVC and RA are thought to generate the motor commands for the different brainstem nuclei that, respectively, control respiration and the syrinx (Suthers and Margoliash, 2002;Fee et al, 2004). Despite its intuitive appeal, a hierarchical view of motor control in the avian song system fails to explain our current results as well as the observed synchronization of premotor activity between left and right HVC (Schmidt, 2003). Given the functional and anatomical organization of the song system, song motor control can be alternatively explained with a recurrent flow of information through the song system.…”

“…Premotor activity within HVC is synchronized between hemispheres during song production (Schmidt, 2003), despite the absence of commissural connections between these two nuclei or any other forebrain song control nuclei (Fig. 1).…”

Temporal Structure in Zebra Finch Song: Implications for Motor Coding

“…Bilateral HVC recordings show brief periods during each motif in which multiunit activity becomes synchronized across hemispheres (Schmidt, 2003). Because there are no interhemispheric connections in the avian forebrain, this synchronization must be induced by HVC afferents.…”

Chilling device slows birdsong

“…f, Stretch of subsyllabic elements for the population of RA cooled birds (n 5 4, 20 syllables), corrected for HVC temperature change. NATURE ARTICLES syllable (and at some acoustic transitions within long complex syllables) 34,35 , probably mediated by feedback pathways from RA to midbrain areas and bilaterally back to HVC 18,19 . Do these episodes reflect actual bilateral synchronization of the HVCs?…”

“…Thus, one interesting possibility is that HVC may contain multiple independent chains 8 (or modules), which may be associated with syllables or long subsyllabic elements 34 . These modules, each of which could run autonomously by virtue of circuit dynamics within HVC, may then be linked together in time by the feedback connections from RA through the thalamus and back to HVC (Supplementary Nature nature07448.3d 13/10/08 13:51:04…”