Mechanisms and time course of vocal learning and consolidation in the adult songbird

Abstract

In songbirds, the basal ganglia outflow nucleus LMAN is a cortical analog that is required for several forms of song plasticity and learning. Moreover, in adults, inactivating LMAN can reverse the initial expression of learning driven via aversive reinforcement. In the present study, we investigated how LMAN contributes to both reinforcement-driven learning and a self-driven recovery process in adult Bengalese finches. We first drove changes in the fundamental frequency of targeted song syllables and compared the effects of inactivating LMAN with the effects of interfering with N-methyl-d-aspartate (NMDA) receptor-dependent transmission from LMAN to one of its principal targets, the song premotor nucleus RA. Inactivating LMAN and blocking NMDA receptors in RA caused indistinguishable reversions in the expression of learning, indicating that LMAN contributes to learning through NMDA receptor-mediated glutamatergic transmission to RA. We next assessed how LMAN's role evolves over time by maintaining learned changes to song while periodically inactivating LMAN. The expression of learning consolidated to become LMAN independent over multiple days, indicating that this form of consolidation is not completed over one night, as previously suggested, and instead may occur gradually during singing. Subsequent cessation of reinforcement was followed by a gradual self-driven recovery of original song structure, indicating that consolidation does not correspond with the lasting retention of changes to song. Finally, for self-driven recovery, as for reinforcement-driven learning, LMAN was required for the expression of initial, but not later, changes to song. Our results indicate that NMDA receptor-dependent transmission from LMAN to RA plays an essential role in the initial expression of two distinct forms of vocal learning and that this role gradually wanes over a multiday process of consolidation. The results support an emerging view that cortical-basal ganglia circuits can direct the initial expression of learning via top-down influences on primary motor circuitry.

A Higher Sensory Brain Region Is Involved in Reversing Reinforcement-Induced Vocal Changes in a Songbird

“…Our work contributes to an area of lesion research that allowed, for example, the identification of hippocampal and cortical areas in the initial acquisition of memories (Scoville and Milner, 1957;Teng and Squire, 1999;Squire et al, 2001;Tse et al, 2007) and long-term memory storage (Takehara et al, 2003;Steffenach et al, 2005;Clark et al, 2011), respectively. The ability of NCM-lesioned birds to learn a song discrimination task contrasts with these typically dissociated roles of mammalian brain areas in either acquisition or late retrieval of memories.…”

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

“…First, LMAN bursting may be especially effective at modulating activity in the song motor nucleus RA, driving fluctuations in song that could function as motor exploration (24-27, 36, 45-47). Second, given recent evidence that LMAN can adaptively bias song output (16,48,49), it is also possible that song-locked bursting contributes to song plasticity directly, by instructing specific changes in the synaptic connections between the premotor nucleus HVC and RA via spike-timing-dependent mechanisms (24,27,36,47,50,51). Third, burst firing might also increase the synchrony of activity across multiple neurons in LMAN, and thus enhance their effectiveness in influencing RA and subsequent song output.…”

Two neural streams, one voice: Pathways for theme and variation in the songbird brain

“…Shifts toward the lower-left corner of the plot indicate that the temporal structure of song becomes less variable following LMAN ablation. that AFP activity is necessary for birds to alter the spectral structure of their vocal output in a goal-directed fashion (Tumer and Brainard, 2007;Andalman and Fee, 2009;Warren et al, 2011;Charlesworth et al, 2012;Ali et al, 2013).…”