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

Abstract

Brainstem nuclei have well established roles in generating nonlearned rhythmic behaviors or as output pathways for more complex, forebrain-generated behaviors. However, the role of the brainstem in providing information to the forebrain that is used to initiate or assist in the control of complex behaviors is poorly understood. In this study, we used electrical microstimulation in select nuclei of the avian song system combined with recordings of acoustic and respiratory output to examine how forebrain and brainstem nuclei interact in the generation of learned vocal motor sequences. We found that brief stimulation in the forebrain nuclei HVC (used as a proper name) and RA (robust nucleus of the arcopallium) caused a short-latency truncation of ongoing song syllables, which ultimately led to a cessation of the ongoing motor sequence. Stimulation within the brainstem inspiratory-related nucleus paraambigualis, which receives input from RA and projects back to HVC via the thalamus, caused syllable truncations and interruptions similar to those observed in HVC and RA. In contrast, stimulation in the tracheosyringal portion of the hypoglossal nucleus, which innervates the syrinx (the avian vocal organ) but possesses no known projections back into the song system, did not cause any significant changes in the song motor pattern. These findings suggest that perturbation of premotor activity in any nucleus within the recurrent song system motor network will disrupt the ongoing song motor sequence. Given the anatomical organization of this network, our results are consistent with a model in which the brainstem respiratory nuclei form an integral part of the song motor programming network by providing timing signals to song control nuclei in the forebrain.

Central pattern generators for social vocalization: Androgen-dependent neurophysiological mechanisms

“…During the 1970s, several reports mapped vocal pathways and sites of steroid binding in several species of songbirds, and essentially launched three decades of investigations into steroid influences on the neural mechanisms of birdsong (Zigmond et al, 1973;Arnold et al, 1976;Nottebohm and Arnold, 1976;. While recent analyses have approached the songbird vocal system mainly from a CPG perspective (e.g., Sturdy et al, 2003;Ashmore et al, 2005;Leonardo and Fee, 2005;Solis and Perkel, 2005), studies of androgen influences on the electroresponsive properties of neurons within the avian song system are just beginning (e.g., White et al, 1999;Park et al, 2005;Meitzen et al, 2007). Investigations dating from the 1970s also began to map a vocal control system among mammals (Jürgens, 2002;Jürgens and Hage, 2006).…”

Auditory-induced neural dynamics in sensory-motor circuitry predict learned temporal and sequential statistics of birdsong

“…. → HVC) (45), and activation due to sensory feedback (29,35,46). Our observation that the dynamics of poststimulus activity were slowed by ∼10 ms relative to the expected timing of song [for both temporal tuning (Fig.…”

“…3 D and E) and peak predictive strength (Fig. 4B)] also suggests that the song generation network is in a different state during singing, perhaps resulting from different neuromodulatory tone (47), or from additional excitatory inputs that are not activated during playback experiments (32)(33)(34)(35)45).…”

Auditory–vocal mirroring in songbirds

“…In fact, the product of several decades of research by a wide variety of groups has provided considerable insights into the circuit mechanisms that underlie the expression of singing-related and auditory-evoked activity of auditory -vocal mirror neurons. Similar to the manner in which mammalian motor cortex is recurrently connected to brainstem and basal ganglia structures, the songbird HVC is recurrently connected with downstream elements in the SMP and the AFP, as well as with neurons in the auditory telencephalon [79][80][81][82][83][84][85]. Thus, the functional properties of HVC mirror neurons must in some manner arise through complex and potentially reciprocal interactions with other brain regions.…”