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Allison J Doupe

Publications and source records attributed to Allison J Doupe.

7 recordsLinked to original sources

Temporal processing and adaptation in the songbird auditory forebrain.

Songbird auditory neurons must encode the dynamics of natural sounds at many volumes. We investigated how neural coding depends on the distribution of stimulus intensities. Using reverse-correlation, we modeled responses to amplitude-modulated sounds as the output of a linear filter and a nonlinear gain function, then asked how filters and nonlinearities depend on the stimulus mean and variance. Filter shape depended strongly on mean amplitude (volume): at low mean, most neurons integrated sound over many milliseconds, while at high mean, neurons responded more to local changes in amplitude. Increasing the variance (contrast) of amplitude modulations had less effect on filter shape but decreased the gain of firing in most cells. Both filter and gain changes occurred rapidly after a change in statistics, suggesting that they represent nonlinearities in processing. These changes may permit neurons to signal effectively over a wider dynamic range and are reminiscent of findings in other sensory systems.

Acclimatization↗

Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song.

Cortical-basal ganglia circuits have a critical role in motor control and motor learning. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia-forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.

Acoustic Stimulation↗

Birdbrains could teach basal ganglia research a new song.

Recent advances in anatomical, physiological and histochemical characterization of avian basal ganglia neurons and circuitry have revealed remarkable similarities to mammalian basal ganglia. A modern revision of the avian anatomical nomenclature has now provided a common language for studying the function of the cortical-basal-ganglia-cortical loop, enabling neuroscientists to take advantage of the specialization of basal ganglia areas in various avian species. For instance, songbirds, which learn their vocal motor behavior using sensory feedback, have specialized a portion of their cortical-basal ganglia circuitry for song learning and production. This discrete circuit dedicated to a specific sensorimotor task could be especially tractable for elucidating the interwoven sensory, motor and reward signals carried by basal ganglia, and the function of these signals in task learning and execution.

Animals↗

Is the songbird Area X striatal, pallidal, or both? An anatomical study.

Anatomical and neurophysiological studies have established that Area X, a songbird nucleus essential for vocal learning, is a basal ganglia structure, with mammalian striatal properties. However, Area X also sends a gamma-aminobutyric acid (GABA)ergic projection to the medial portion of the dorsolateral thalamus (DLM), a projection characteristic of the pallidum. These findings suggested that Area X contains both striatal and pallidal neurons. To test this hypothesis further, we investigated the neurochemistry and connectivity of Area X and its projections by using neurotransmitter antibodies, in combination with tracing studies. Like the mammalian striatum, Area X contains small enkephalin- and substance P-immunopositive neurons. Choline acetyltransferase-positive cells of Area X do not retrogradely label from DLM and are probably cholinergic interneurons similar to those in mammals. Like pallidal cells, large GABAergic cells project from Area X to the thalamus, but they also contain enkephalin, a characteristic of striatal neurons projecting to indirect pathway pallidal neurons. Moreover, many Area X cells are labeled with the pallidal marker Nkx2.1, but these do not include any thalamus-projecting neurons, suggesting that the projection cells are not of pallidal embryonic origin. Thus, although Area X combines both striatal and pallidal features, it is not a simple recapitulation of the mammalian circuit or of the avian lateral striatopallidal pathway: some individual Area X neurons may function as pallidal-like projection neurons but have striatal characteristics as well. Such heterogeneity of basal ganglia circuitry, both within and across species, may be facilitated by the developmental history of basal ganglia, which involves extensive migration and cellular intermixing.

Animals↗

Cellular, circuit, and synaptic mechanisms in song learning.

Songbirds, much like humans, learn their vocal behavior, and must be able to hear both themselves and others to do so. Studies of the brain areas involved in singing and song learning could reveal the underlying neural mechanisms. Here we describe experiments that explore the properties of the songbird anterior forebrain pathway (AFP), a basal ganglia-forebrain circuit known to be critical for song learning and for adult modification of vocal output. First, neural recordings in anesthetized, juvenile birds show that auditory AFP neurons become selectively responsive to the song stimuli that are compared during sensorimotor learning. Individual AFP neurons develop tuning to the bird's own song (BOS), and in many cases to the tutor song as well, even when these stimuli are manipulated to be very different from each other. Such dual selectivity could be useful in the BOS-tutor song comparison critical to song learning. Second, simultaneous neural recordings from the AFP and its target nucleus in the song motor pathway in anesthetized adult birds reveal correlated activity that is preserved through multiple steps of the circuits for song, including the AFP. This suggests that the AFP contains highly functionally interconnected neurons, an architecture that can preserve information about the timing of firing of groups of neurons. Finally, in vitro studies show that recurrent synapses between neurons in the AFP outflow nucleus, which are expected to contribute importantly to AFP correlation, can undergo activity-dependent and timing-sensitive strengthening. This synaptic enhancement appears to be restricted to birds in the sensory critical and early sensorimotor phases of learning. Together, these studies show that the AFP contains cells that reflect learning of both BOS and tutor song, as well as developmentally regulated synaptic and circuit mechanisms well-suited to create temporally organized assemblies of such cells. Such experience-dependent sensorimotor assemblies are likely to be critical to the AFP's role in song learning. Moreover, studies of such mechanisms in this basal ganglia circuit specialized for song may shed light more generally on how basal ganglia circuits function in guiding motor learning using sensory feedback signals.

Animals↗

Propagation of correlated activity through multiple stages of a neural circuit.

The timing of spikes can carry information, for instance, when the temporal pattern of firing across neurons results in correlated activity. However, in part because central synapses are unreliable, correlated activity has not been observed to propagate through multiple subsequent stages in neural circuits, although such propagation has frequently been used in theoretical models. Using simultaneous single-unit and multiunit recordings from two or three vocal control nuclei of songbirds, measurement of coherency and time delays, and manipulation of neural activity, we provide evidence here for preserved correlation of activity through multiple steps of the neural circuit for song, including a basal ganglia circuit and its target vocal motor pathway. This suggests that these pathways contain highly functionally interconnected neurons and represent a neural architecture that can preserve information about the timing of firing of groups of neurons. Because the interaction of these song pathways is critical to vocal learning, the preserved correlation of activity may be important to the learning and production of sequenced motor acts and could be a general feature of basal ganglia-cortical interaction.

Acoustic Stimulation↗

What songbirds teach us about learning.

Bird fanciers have known for centuries that songbirds learn their songs. This learning has striking parallels to speech acquisition: like humans, birds must hear the sounds of adults during a sensitive period, and must hear their own voice while learning to vocalize. With the discovery and investigation of discrete brain structures required for singing, songbirds are now providing insights into neural mechanisms of learning. Aided by a wealth of behavioural observations and species diversity, studies in songbirds are addressing such basic issues in neuroscience as perceptual and sensorimotor learning, developmental regulation of plasticity, and the control and function of adult neurogenesis.

Aging↗