Rapid Interhemispheric Switching during Vocal Production in a Songbird

Abstract

To generate complex bilateral motor patterns such as those underlying birdsong, neural activity must be highly coordinated across the two cerebral hemispheres. However, it remains largely elusive how this coordination is achieved given that interhemispheric communication between song-control areas in the avian cerebrum is restricted to projections received from bilaterally connecting areas in the mid- and hindbrain. By electrically stimulating cerebral premotor areas in zebra finches, we find that behavioral effectiveness of stimulation rapidly switches between hemispheres. In time intervals in which stimulation in one hemisphere tends to distort songs, stimulation in the other hemisphere is mostly ineffective, revealing an idiosyncratic form of motor dominance that bounces back and forth between hemispheres like a virtual ping-pong ball. The intervals of lateralized effectiveness are broadly distributed and are unrelated to simple spectral and temporal song features. Such interhemispheric switching could be an important dynamical aspect of neural coordination that may have evolved from simpler pattern generator circuits.

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

“…In combination, our estimate of the LMAN loop delay is in the range of 32-154 ms, with a median of 56 ms, similar to the loop delay estimate in HVC (26)(27)(28)(29)(30)(31). The theory (SI Methods) predicts that the mirroring offset in randomly firing premotor areas such as LMAN is within the range of short loop delays (because nearby pre-post spike pairs are expected to lead to strong synaptic potentiation, thus favoring short delays (24).…”

“…Accordingly, we expect to find a causal inverse upstream of LMAN (23,24). Indeed, in HVC neurons the mirroring offset between motor-related spiking and song-playback evoked spiking is less than 10 ms (25), much less than the roughly 40-ms loop delay of HVC estimated using electrical stimulation of HVC and using auditory stimulation of the ear (26)(27)(28)(29)(30)(31). By contrast, mirroring offsets in LMAN have not been quantified yet, leaving it open as to whether they provide evidence for causal inverses.…”

Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities

“…This same relationship has been demonstrated in the ring dove (Streptopelia risoria), a nonpasserine with a single vocal source (a tracheal syrinx) [39]. In songbirds, sound production is more complex, as they have two independently controlled sound sources (a tracheo-bronchial syrinx), the control of which often requires rapid bilateral coordination of central song control nuclei, respiratory and syringeal muscles, and the dynamic adjustment of the upper vocal tract to match the frequencies produced by either of the sides of the syrinx [40][41][42][43]. However, despite this more complex vocal production system, there is scattered evidence from at least four songbird species for a positive correlation between song frequency and amplitude [44][45][46][47].…”

Components of the Language-Ready Brain

“…The hypothesis I wish to put forward is the following: it is the structure of the Corpus Callosum that makes humans' brains display a sophisticated, selective asymmetry: in the anterior/medial cortex, where callosal fibers are narrow and intrahemispheric connectivity is enhanced, asymmetry is expressed at the level of small-world networks, i.e., cognitive functions appear to be lateralized as modules (e.g., the default network in the left and the attentional in the right hemisphere: Wang et al, 2008;; in the posterior cortex, there is no such asymmetry, as visual, auditory, and motor functions appear in both hemispheres. What makes the posterior cortex asymmetrical is to be found in the hemispheres' refinement toward processing input of specific 'sampling rate' (temporal-faster rate sampling executed in the left hemisphere and spectral-slower rate in the right).…”