Regulation of vocal precision by noradrenergic modulation of a motor nucleus.

Recent theories of norepinephrine (NE) function suggest that NE modulates the transition between stereotyped, goal-directed behavior and more variable, exploratory behaviors that facilitate learning and adaptation. We provide evidence for context-dependent switching by NE that is analogous to this explore/exploit strategy in the vocal system of the zebra finch (Taeniopygia guttata). Stimulation of the locus coeruleus, the major source of NE in the brain, decreases song trial-to-trial variability, transforming the variable, exploratory "undirected" song into song that resembles the more stereotyped, exploitative "directed" song that males sing to females. This behavioral switch is mediated by NE acting directly on a cortical motor nucleus that integrates inputs from a premotor cortical nucleus and a basal ganglia circuit necessary for vocal motor learning. These findings suggest that NE can act directly on the motor system to influence the transition between exploratory and exploitative behavioral strategies.NEW & NOTEWORTHY Norepinephrine (NE) function is often implicated in regulating arousal levels. Recent theory suggests that the noradrenergic system also regulates the optimization of behavior with respect to reward maximization by controlling a switch between exploration and exploitation of the specific actions that yield greatest utility. We show in the songbird that NE can act directly on a cortical motor area and cause a switch between exploratory and exploitative behavior.

Pupil diameter encodes the idiosyncratic, cognitive complexity of belief updating.

Pupils tend to dilate in response to surprising events, but it is not known whether these responses are primarily stimulus driven or instead reflect a more nuanced relationship between pupil-linked arousal systems and cognitive expectations. Using an auditory adaptive decision-making task, we show that evoked pupil diameter is more parsimoniously described as signaling violations of learned, top-down expectations than changes in low-level stimulus properties. We further show that both baseline and evoked pupil diameter is modulated by the degree to which individual subjects use these violations to update their subsequent expectations, as reflected in the complexity of their updating strategy. Together these results demonstrate a central role for idiosyncratic cognitive processing in how arousal systems respond to new inputs and, via our complexity-based analyses, offer a potential framework for understanding these effects in terms of both inference processes aimed to reduce belief uncertainty and more traditional notions of mental effort.

Normative evidence accumulation in unpredictable environments.

In our dynamic world, decisions about noisy stimuli can require temporal accumulation of evidence to identify steady signals, differentiation to detect unpredictable changes in those signals, or both. Normative models can account for learning in these environments but have not yet been applied to faster decision processes. We present a novel, normative formulation of adaptive learning models that forms decisions by acting as a leaky accumulator with non-absorbing bounds. These dynamics, derived for both discrete and continuous cases, depend on the expected rate of change of the statistics of the evidence and balance signal identification and change detection. We found that, for two different tasks, human subjects learned these expectations, albeit imperfectly, then used them to make decisions in accordance with the normative model. The results represent a unified, empirically supported account of decision-making in unpredictable environments that provides new insights into the expectation-driven dynamics of the underlying neural signals.

Development of temporal structure in zebra finch song.

Zebra finch song has provided an excellent case study in the neural basis of sequence learning, with a high degree of temporal precision and tight links with precisely timed bursting in forebrain neurons. To examine the development of song timing, we measured the following four aspects of song temporal structure at four age ranges between 65 and 375 days posthatch: the mean durations of song syllables and the silent gaps between them, timing variability linked to song tempo, timing variability expressed independently across syllables and gaps, and transition probabilities between consecutive syllable pairs. We found substantial increases in song tempo between 65 and 85 days posthatch, due almost entirely to a shortening of gaps. We also found a decrease in tempo variability, also specific to gaps. Both the magnitude of the increase in tempo and the decrease in tempo variability were correlated on gap-by-gap basis with increases in the reliability of corresponding syllable transitions. Syllables had no systematic increase in tempo or decrease in tempo variability. In contrast to tempo parameters, both syllables and gaps showed an early sharp reduction in independent variability followed by continued reductions over the first year. The data suggest that links between syllable-based representations are strengthened during the later parts of the traditional period of song learning and that song rhythm continues to become more regular throughout the first year of life. Similar learning patterns have been identified in human sequence learning, suggesting a potentially rich area of comparative research.

A generative model for measuring latent timing structure in motor sequences.

Motor variability often reflects a mixture of different neural and peripheral sources operating over a range of timescales. We present a statistical model of sequence timing that can be used to measure three distinct components of timing variability: global tempo changes that are spread across the sequence, such as might stem from neuromodulatory sources with widespread influence; fast, uncorrelated timing noise, stemming from noisy components within the neural system; and timing jitter that does not alter the timing of subsequent elements, such as might be caused by variation in the motor periphery or by measurement error. In addition to quantifying the variability contributed by each of these latent factors in the data, the approach assigns maximum likelihood estimates of each factor on a trial-to-trial basis. We applied the model to adult zebra finch song, a temporally complex behavior with rich structure on multiple timescales. We find that individual song vocalizations (syllables) contain roughly equal amounts of variability in each of the three components while overall song length is dominated by global tempo changes. Across our sample of syllables, both global and independent variability scale with average length while timing jitter does not, a pattern consistent with the Wing and Kristofferson (1973) model of sequence timing. We also find significant day-to-day drift in all three timing sources, but a circadian pattern in tempo only. In tests using artificially generated data, the model successfully separates out the different components with small error. The approach provides a general framework for extracting distinct sources of timing variability within action sequences, and can be applied to neural and behavioral data from a wide array of systems.

Linear and nonlinear auditory response properties of interneurons in a high-order avian vocal motor nucleus during wakefulness.

Motor-related forebrain areas in higher vertebrates also show responses to passively presented sensory stimuli. However, sensory tuning properties in these areas, especially during wakefulness, and their relation to perception, are poorly understood. In the avian song system, HVC (proper name) is a vocal-motor structure with auditory responses well defined under anesthesia but poorly characterized during wakefulness. We used a large set of stimuli including the bird's own song (BOS) and many conspecific songs (CON) to characterize auditory tuning properties in putative interneurons (HVC(IN)) during wakefulness. Our findings suggest that HVC contains a diversity of responses that vary in overall excitability to auditory stimuli, as well as bias in spike rate increases to BOS over CON. We used statistical tests to classify cells in order to further probe auditory responses, yielding one-third of neurons that were either unresponsive or suppressed and two-thirds with excitatory responses to one or more stimuli. A subset of excitatory neurons were tuned exclusively to BOS and showed very low linearity as measured by spectrotemporal receptive field analysis (STRF). The remaining excitatory neurons responded well to CON stimuli, although many cells still expressed a bias toward BOS. These findings suggest the concurrent presence of a nonlinear and a linear component to responses in HVC, even within the same neuron. These characteristics are consistent with perceptual deficits in distinguishing BOS from CON stimuli following lesions of HVC and other song nuclei and suggest mirror neuronlike qualities in which "self" (here BOS) is used as a referent to judge "other" (here CON).

Behavioral measurements of a temporally precise motor code for birdsong.

There are conflicting data on the timescale for the representation of adult zebra finch song. Acoustic structure and perturbation studies suggest that song is divided into discrete vocal elements, or syllables, lasting 50-200 ms. However, recordings in premotor telencephalic nucleus HVC (used as proper name) and RA (robust nucleus of arcopallium) suggest that song is represented by sparse, fine-grained bursting on the 5-10 ms timescale. We previously found patterns of timing variability that distinguish individual syllables and repeat across multiple 500- to 1000-ms-long motifs (Glaze and Troyer, 2006). Here, we extend our methods to analyze whether this is attributable to a syllable-based code or representations on a finer timescale. We find evidence for the latter. First, identity-dependent timing is dominated by independent variability in notes, finer song segments that compose a syllable; for example, the length of a note is no more correlated with other notes in the same syllable than it is with notes in other syllables. For a subset of notes, clear modulation in spectral structure allowed for accurate timing measurements on the 5-10 ms timescale. Temporal independence holds at this scale as well: the length of an individual 5-10 ms song slice is correlated with the same slice repeated 500-1000 ms later, yet is independent of neighboring slices. We propose that such fine-grained, persistent changes in song tempo result from an interaction between slow modulatory factors and precisely timed, sparse bursting in HVC and RA.

Temporal structure in zebra finch song: implications for motor coding.

Adult zebra finch songs consist of stereotyped sequences of syllables. Although some behavioral and physiological data suggest that songs are structured hierarchically, there is also evidence that they are driven by nonhierarchical, clock-like bursting in the premotor nucleus HVC (used as a proper name). In this study, we developed a semiautomated template-matching algorithm to identify repeated sequences of syllables and a modified dynamic time-warping algorithm to make fine-grained measurements of the temporal structure of song. We find that changes in song length are expressed across the song as a whole rather than resulting from an accumulation of independent variance during singing. Song length changes systematically over the course of a day and is related to the general level of bird activity as well as the presence of a female. The data also show patterns of variability that suggest distinct mechanisms underlying syllable and gap lengths: as tempo varies, syllables stretch and compress proportionally less than gaps, whereas syllable-syllable and gap-gap correlations are significantly stronger than syllable-gap correlations. There is also increased temporal variability at motif boundaries and especially strong positive correlations between the same syllables sung in different motifs. Finally, we find evidence that syllable onsets may have a special role in aligning syllables with global song structure. Generally, the timing data support a hierarchical view in which song is composed of smaller syllable-based units and provide a rich set of constraints for interpreting the results of physiological recordings.