Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds

Abstract

Accurate timing is a critical aspect of motor control, yet the temporal structure of many mature behaviors emerges during learning from highly variable exploratory actions. How does a developing brain acquire the precise control of timing in behavioral sequences? To investigate the development of timing, we analyzed the songs of young juvenile zebra finches. These highly variable vocalizations, akin to human babbling, gradually develop into temporally-stereotyped adult songs. We find that the durations of syllables and silences in juvenile singing are formed by a mixture of two distinct modes of timing – a random mode producing broadly-distributed durations early in development, and a stereotyped mode underlying the gradual emergence of stereotyped durations. Using lesions, inactivations, and localized brain cooling we investigated the roles of neural dynamics within two premotor cortical areas in the production of these temporal modes. We find that LMAN (lateral magnocellular nucleus of the nidopallium) is required specifically for the generation of the random mode of timing, and that mild cooling of LMAN causes an increase in the durations produced by this mode. On the contrary, HVC (used as a proper name) is required specifically for producing the stereotyped mode of timing, and its cooling causes a slowing of all stereotyped components. These results show that two neural pathways contribute to the timing of juvenile songs, and suggest an interesting organization in the forebrain, whereby different brain areas are specialized for the production of distinct forms of neural dynamics.

Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex

“…Song amplitude was calculated as previously described (Aronov et al, 2011). Briefly, the microphone signal was bandpass filtered, rectified, and smoothed.…”

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing, production and learning

“…The descending motor pathway is made up of the telencephalic nucleus HVC (used as a proper name) and its efferent target RA (the robust nucleus of the arcopallium), which sends projections to respiratory and vocal motor nuclei in the brainstem (Wild et al, 2000; Wild, 2004). Converging evidence from lesions (Simpson and Vicario, 1990; Aronov et al, 2008), electrical stimulation (Vu et al, 1994), localized cooling (Long and Fee, 2008; Aronov et al, 2011), and single cell recordings (Hahnloser et al, 2002, 2006) indicate that HVC drives the descending motor pathway to shape many of the spectrotemporal features of song. The anterior forebrain pathway consists of a basal ganglia–thalamo-cortical circuit that indirectly links HVC to RA and is critical for song learning (Brainard and Doupe, 2000a).…”

Brain heating induced by near-infrared lasers during multiphoton microscopy

“…In two-photon imaging, doubling the laser power quadruples the signal rate achievable from a given focal pattern. However, light absorption heats brain tissue, which can change neural function (Aronov et al 2011;Hodgkin and Katz 1949;Kiyatkin 2007;Milburn et al 1995;Stujenske et al 2015). Heating is of particular concern for multiphoton techniques, because simultaneous absorption of two coherent photons occurs with low probability and requires high light intensities.…”

“…Even relatively low illumination powers can increase neuronal firing rates (5 mW at 532 nm; Stujenske et al 2015). Neural circuit dynamics are also affected by both manipulations and natural variations in brain temperature (Aronov and Fee 2012;Aronov et al 2011), and febrile seizures occur in children with elevated brain temperatures (Pavlidou et al 2013). Heating can cause lasting damage to tissues, and the brain is especially sensitive to such damage (Dewhirst et al 2003).…”