Electrical stimulation in forebrain nuclei elicits learned vocal patterns in songbirds

Brainstem motor structures send output commands to the periphery and are dynamically modulated by telencephalic inputs. Little is known, however, about ascending brainstem control of forebrain motor structures. Here, we provide the first evidence for bottom-up activation of forebrain motor centers by the respiratory brainstem. We show that, in the avian vocal control system, activation of the brainstem inspiratory nucleus paraambigualus (PAm), a likely homolog of the mammalian rostral ventral respiratory group, can drive neural activity bilaterally in the forebrain vocal control nuclei HVC (used as a proper name) and the robust nucleus of the arcopallium (RA). Furthermore, this activation is abolished by lesions of nucleus uvaeformis (Uva), a thalamic nucleus necessary for song production. We identify a type of bursting neuron within PAm whose activity is correlated, in an Uva dependent manner, to bursting activity in RA, rather than to the respiratory rhythm, and is robustly active during the production of stimulus evoked vocalizations. Because this ascending input results in cross-hemisphere activation, our results suggest a crucial role for the respiratory brainstem in coordinating forebrain motor centers during vocal production.

Section: Methodsmentioning

confidence: 99%

Bottom-Up Activation of the Vocal Motor Forebrain by the Respiratory Brainstem

Ashmore¹,

Renk²,

Schmidt³

2008

“…Introductory notes ("i") precede the first motif and, together with the multiple motifs, comprise a song bout. Vicario and Simpson, 1995). Stimuli consisted of trains of 100-s-long monophasic pulses.…”

Section: Methodsmentioning

confidence: 99%

“…As part of the motor pathway, HVC is necessary for singing, has the appropriate connectivity to influence song output (Nottebohm et al, 1976), and exhibits patterned premotor activity during singing (McCasland, 1987;Yu and Margoliash, 1996;Hahnloser et al, 2002). In addition, in vivo stimulation studies implicate HVC as a part of the CPG network for song: stimulating HVC in a singing bird resets the song pattern (Vu et al, 1994), and there is some suggestion that high-frequency stimulation delivered to HVC in quiescent birds can elicit vocalizations (Vu et al, 1994;Vicario and Simpson, 1995). Thus, patterned activity in HVC accompanies song production.…”

Section: Introductionmentioning

confidence: 99%

Rhythmic Activity in a Forebrain Vocal Control NucleusIn Vitro

Solis¹,

Perkel²

2005

The learned vocalizations of songbirds constitute a rhythmic behavior that is thought to be governed by a central pattern generator and that is accompanied by highly patterned neural activity. Phasic premotor activity is observed during singing in HVC [used as a proper name following the nomenclature of Reiner et al. (2004)], a telencephalic song system nucleus that is essential for song production. Moreover, HVC neurons display phasic patterns of auditory activity in response to song stimulation. To address the cellular basis of pattern generation in HVC, we investigated its rhythm-generating abilities.We report here the induction of sustained, rhythmic activity patterns in HVC when isolated in vitro. Brief, high-frequency stimulation evoked repetitive postsynaptic potentials (PSPs) and local field potentials (LFPs) from HVC neurons recorded in a brain slice preparation made from adult male zebra finches. These rhythmic events were sustained for seconds in the absence of ongoing, phasic stimulation, and they had temporal properties similar to those of syllable occurrence within zebra finch song. Paired recordings revealed synchrony between repetitive PSP and LFP occurrence, indicating that a population of cells participates in this patterned activity. The PSPs resulted from multiple, coordinated, fast-glutamatergic, synaptic inputs. Moreover, their occurrence and timing relied on inhibitory synaptic transmission. Thus, HVC itself has rhythmic abilities that could influence the timing of neural activity over relatively long time windows. These rhythmic properties may contribute to song production or perception in vivo.

“…In the song system, several telencephalic nuclei are critical to song behavior, and lesions of these, such as the forebrain nucleus HVC (used as a proper name), or of one of its efferent targets, the robust nucleus of the arcopallium (RA), disrupt or prevent song production (Nottebohm et al, 1976;Simpson and Vicario, 1990;Halle et al, 2003). Electrical microstimulation of these structures also affects song production (Vicario and Simpson, 1995;Fee et al, 2004) and, when applied to HVC in particular, stops or restarts ongoing song in both auditorily intact and experimentally deafened birds, implying that the stimulation effects cannot be attributed to auditory feedback (Vu et al, 1994. The descending projections of RA terminate in brainstem nuclei that are necessary for song production (Vicario, 1991), namely the tracheosyringal portion of the hypoglossal nucleus (nXIIts) that controls muscles of the syrinx, the avian vocal organ, and medullary premotor nuclei that, via their spinal projections, modulate the activity of inspiratory and expiratory motor neurons (Nottebohm et al, 1976(Nottebohm et al, , 1982Wild, 1993a,b;Reinke and Wild, 1998) (Fig.…”

Section: Introductionmentioning

confidence: 99%

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

Ashmore

Wild²,

Schmidt³

2005

125

140

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.