Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity

Disinhibition of the thalamus remains the primary model of information transfer between the basal ganglia and the cortex. Yet in apparent conflict with this model, the globus pallidus, a GABAergic basal ganglia output structure, often exhibits marked increases in firing rate during movement. To investigate the translation of pallidal activity and its relay through the thalamus, we explored a basal ganglia-thalamic pathway essential for song learning in songbirds. We found that single units in the thalamic nucleus DLM of urethaneanesthetized adult male zebra finches responded selectively to playback of the bird's own song, like neurons in its upstream and downstream nuclei. Because the pallidal input to these neurons forms giant calyx-like synapses, we were able to record extracellular signals from these presynaptic terminals as well. Pallidal units were distinctly excited by song playback, suggesting an increase in GABAergic transmission in the thalamus during sensory processing. However, this overall increased firing rate was phasic, punctuated by rapid decelerations in firing rate. In several cases, we were able to record presynaptic and postsynaptic units simultaneously. Correlating the presynaptic and postsynaptic activity, we found that disinhibition of thalamus may entail pallidal firing rate decelerations rather than simple long pauses in spontaneous activity, as has long been assumed.

Section: Discussionmentioning

confidence: 99%

Pallidal Neuron Activity Increases during Sensory Relay through Thalamus in a Songbird Circuit Essential for Learning

Person

Perkel

2007

“…The lack of topographic organization seen in 35 d DF/WN birds suggests that auditory input may directly affect the initial restriction of axonal connections of lMAN core neurons to different subregions of RA between 20 d and 35 d. Interestingly, RA-projecting neurons in lMAN core respond selectively to a bird's own song (Rosen and Mooney, 2000), suggesting that auditory deprivation may act directly on these neurons to alter experience-dependent mechanisms that normally regulate the topographic organization of this projection. Alternatively, the absence of normal auditory input may indirectly affect the development of topographic organization in the lMAN core 3 RA circuit.…”

Section: Discussionmentioning

confidence: 99%

“…The RA contains a myotopic map of the syrinx (Vicario, 1991;Wild, 1993Wild, , 1997, and topography within the lMAN core 3 RA circuit may represent the organization of muscles within the syrinx (Johnson et al, 1995;Vates and Nottebohm, 1995). Topographic specificity within lMAN core may also represent complex acoustic features of the songs sung by male zebra finches, which become tuned to birds' own songs during development, or a combination of different factors important for vocal learning and auditory-motor integration Jarvis and Nottebohm, 1997;Jin and Clayton, 1997;Solis and Doupe, 1997;Rosen and Mooney, 2000). During early stages of song learning, juvenile swamp sparrows sing a large number of notes (subsong), of which only a small number are retained in the adult song.…”

Section: Discussionmentioning

confidence: 99%

The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches

Iyengar

Bottjer

2002

The initial establishment of topographic mapping within developing neural circuits is thought to be shaped by innate mechanisms and is primarily independent of experience. Additional refinement within topographic maps leads to precise matching between presynaptic and postsynaptic neurons and is thought to depend on experiential factors during specific sensitive periods in the animal's development. In male zebra finches, axonal projections of the cortical lateral magnocellular nucleus of the anterior neostriatum (lMAN) are critically important for vocal learning. Overall patterns of topographic organization in the majority of these circuits are adult-like throughout the sensitive period for vocal learning and remain stable despite large-scale functional and morphological changes. However, topographic organization within the projection from the core subregion of lMAN (lMAN core ) to the motor cortical robust nucleus of the archistriatum (RA) is lacking at the onset of song development and emerges during the early stages of vocal learning. To study the effects of song-related experience on patterns of axonal connectivity within different song-control circuits, we disrupted song learning by deafening juvenile zebra finches or exposing them to loud white noise throughout the sensitive period for song learning. Depriving juvenile birds of normal auditory experience delayed the emergence of topographic specificity within the lMAN core 3RA circuit relative to age-matched controls, whereas topographic organization within all other projections to and from lMAN was not affected. The projection from lMAN core to RA therefore provides an unusual example of experience-dependent modification of large-scale patterns of brain circuitry, in the sense that auditory deprivation influences the development of overall topographic organization in this pathway.

“…General methods for these procedures have been described previously (Mooney, 2000;Rosen and Mooney, 2000).…”

Section: Methodsmentioning

confidence: 99%

Synaptic Transformations Underlying Highly Selective Auditory Representations of Learned Birdsong

Coleman¹,

Mooney²

2004

107

138

Stimulus-specific neuronal responses are a striking characteristic of several sensory systems, although the synaptic mechanisms underlying their generation are not well understood. The songbird nucleus HVC (used here as a proper name) contains projection neurons (PNs) that fire temporally sparse bursts of action potentials to playback of the bird's own song (BOS) but are essentially silent when presented with other acoustical stimuli. To understand how such remarkable stimulus specificity emerges, it is necessary to compare the auditory-evoked responsiveness of the afferents of HVC with synaptic responses in identified HVC neurons. We found that inactivating the interfacial nucleus of the nidopallium (NIf) could eliminate all auditory-evoked subthreshold activity in both HVC PN types, consistent with NIf serving as the major auditory afferent of HVC. Simultaneous multiunit extracellular recordings in NIf and intracellular recordings in HVC revealed that NIf population activity and HVC subthreshold responses were similar in their selectivity for BOS and that NIf spikes preceded depolarizations in all HVC cell types. These results indicate that information about the BOS as well as other auditory stimuli is transmitted synaptically from NIf to HVC. Unlike HVC PNs, however, HVC-projecting NIf neurons fire throughout playback of BOS as well as non-BOS stimuli. Therefore, temporally sparse BOS-evoked firing and enhanced BOS selectivity, manifested as an absence of suprathreshold responsiveness to non-BOS stimuli, emerge in HVC. The transformation to a sparse auditory representation parallels differences in NIf and HVC activity patterns seen during singing, which may point to a common mechanism for encoding sensory and motor representations of song.