Characterization of Synaptically Connected Nuclei in a Potential Sensorimotor Feedback Pathway in the Zebra Finch Song System

Abstract

Birdsong is a learned behavior that is controlled by a group of identified nuclei, known collectively as the song system. The cortical nucleus HVC (used as a proper name) is a focal point of many investigations as it is necessary for song production, song learning, and receives selective auditory information. HVC receives input from several sources including the cortical area MMAN (medial magnocellular nucleus of the nidopallium). The MMAN to HVC connection is particularly interesting as it provides potential sensorimotor feedback to HVC. To begin to understand the role of this connection, we investigated the physiological relation between MMAN and HVC activity with simultaneous multiunit extracellular recordings from these two nuclei in urethane anesthetized zebra finches. As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC. Like HVC, MMAN responds to auditory playback of the bird's own song (BOS), but had little response to reversed BOS or conspecific song. Stimulation of MMAN resulted in evoked activity in HVC, indicating functional excitation from MMAN to HVC. However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC. Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals. We hypothesize that MMAN may play a role in motor reinforcement or coordination, or may provide modulatory input to the song system about the internal state of the animal as it receives input from the hypothalamus.

Motor Origin of Precise Synaptic Inputs onto Forebrain Neurons Driving a Skilled Behavior

“…Fat and muscles were pulled to the side and the tracheosyringeal nerve was isolated with fine forceps. A 3-5 mm length of nerve was removed, and the incision into the skin was sutured (Vicario, 1991;Williams and McKibben, 1992).…”

“…For these experiments, we chose to examine the cellular and behavioral consequences of a female call (Fig. 3 A, B), because this stimulus has been shown to have the capacity to perturb ongoing singing behavior (Williams, 2004). Across four birds whose activity was further examined for these experiments, 98 of 290 (33.8%) directed song motifs were accompanied by at least one female call.…”

“…Different RA-projecting HVC (HVC (RA) ) neurons burst at different moments, and together they form a sequence that leads to the patterned activation of song-producing muscles (Fee et al, 2004). HVC receives synaptic inputs from multiple additional sources (Nottebohm et al, 1982;Bauer et al, 2008), which have been shown to carry sensory information (Coleman and Mooney, 2004;Coleman et al, 2007;Ashmore et al, 2008;Bauer et al, 2008;Williams et al, 2012). In certain conditions (sleep and anesthesia), projection neurons within HVC can produce patterned activity elicited by the playback of the bird's own song (BOS) (Lewicki, 1996;Amador et al, 2013;Hamaguchi et al, 2014), indicating that sensory input can affect the motor system by modulating the behavior of those neurons.…”

The respiratory-vocal system of songbirds

“…Interestingly, birds with unilateral Uva lesions, which show similar immediate deficits as bilateral lesioned birds, eventually recover their song. The mechanism of this recovery is not understood but might involve compensation through an alternate pathway that also links RA indirectly back to HVC (RA→DMP (thalamus)→mMAN→HVC) but which in itself is not necessary for song production (Coleman and Vu, 2005; Foster and Bottjer, 2001; Williams et al, 2012). …”

The Basal Ganglia Is Necessary for Learning Spectral, but Not Temporal, Features of Birdsong

“…HVC and RA are also indirectly connected through the Anterior Forebrain Pathway (AFP), a basal ganglia-thalamo-cortical circuit that is critical for song learning, but not essential for producing learned song (Figure 1G) (Bottjer et al, 1984; Scharff and Nottebohm, 1991). A separate basal ganglia circuit, medial to the AFP, receives input from and provides output to HVC (Foster et al, 1997; Kubikova et al, 2007; Williams et al, 2012) (Figure 6A), but the role of this circuit in song learning, if any, remains to be elucidated (Foster and Bottjer, 2001). …”