Dynamic top-down biasing implements rapid adaptive changes to individual movements

Abstract

Complex behaviors depend on the coordinated activity of neural ensembles in interconnected brain areas. The behavioral function of such coordination, often measured as co-fluctuations in neural activity across areas, is poorly understood. One hypothesis is that rapidly varying co-fluctuations may be a signature of moment-by-moment task-relevant influences of one area on another. We tested this possibility for error-corrective adaptation of birdsong, a form of motor learning which has been hypothesized to depend on the top-down influence of a higher-order area, LMAN, in shaping moment-by-moment output from a primary motor area, RA. In paired recordings of LMAN and RA in singing birds, we discovered a neural signature of a top-down influence of LMAN on RA, quantified as an LMAN-leading co-fluctuation between these areas. During learning, this co-fluctuation strengthened in a premotor temporal window linked to the specific movement, sequential context, and acoustic modification associated with learning. Moreover, transient perturbation of LMAN activity specifically within this premotor window caused rapid occlusion of pitch modifications, consistent with LMAN conveying a temporally localized motor-biasing signal. Combined, our results reveal a dynamic top-down influence of LMAN on RA that varies on the rapid timescale of individual movements and is flexibly linked to contexts associated with learning. This finding indicates that inter-area co-fluctuations can be a signature of dynamic top-down influences that support complex behavior and its adaptation.

Lesions in a songbird vocal circuit increase variability in song syntax

“…The variability contributed by lMAN may facilitate motor exploration which forms the basis of pitch adaptations during learning (Andalman and Fee, 2009;Sober and Brainard, 2012;Dhawale, Smith and Ölveczky, 2017). These effects are mediated by top-down influences of lMAN on RA via a recurrent loop that passes through the songbird basal ganglia (Kao, Doupe and Brainard, 2005;Andalman and Fee, 2009;Kojima et al, 2018;Tian, Warren and Brainard, 2022), and are consistent with a role of RA in controlling aspects of syllable acoustic structure.…”