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1.
bioRxiv ; 2024 May 19.
Article in English | MEDLINE | ID: mdl-38798332

ABSTRACT

Neuronal intrinsic excitability is a mechanism implicated in learning and memory that is distinct from synaptic plasticity. Prior work in songbirds established that intrinsic properties (IPs) of premotor basal-ganglia-projecting neurons (HVC X ) relate to learned song. Here we find that temporal song structure is related to specific HVC X IPs: HVC X from birds who sang longer songs including longer invariant vocalizations (harmonic stacks) had IPs that reflected increased post-inhibitory rebound. This suggests a rebound excitation mechanism underlying the ability of HVC X neurons to integrate over long periods of time and represent sequence information. To explore this, we constructed a network model of realistic neurons showing how in-vivo HVC bursting properties link rebound excitation to network structure and behavior. These results demonstrate an explicit link between neuronal IPs and learned behavior. We propose that sequential behaviors exhibiting temporal regularity require IPs to be included in realistic network-level descriptions.

2.
bioRxiv ; 2023 Jan 23.
Article in English | MEDLINE | ID: mdl-36747673

ABSTRACT

In zebra finch, basal ganglia projecting "HVC X " neurons emit one or more spike bursts during each song motif (canonical sequence of syllables), which are thought to be driven in part by a process of spike rebound excitation. Zebra finch songs are highly stereotyped and recent results indicate that the intrinsic properties of HVC X neurons are similar within each bird, vary among birds depending on similarity of the songs, and vary with song errors. We tested the hypothesis that the timing of spike bursts during singing also evince individual-specific distributions. Examining previously published data, we demonstrated that the intervals between bursts of multibursting HVC X are similar for neurons within each bird, in many cases highly clustered at distinct peaks, with the patterns varying among birds. The fixed delay between bursts and different times when neurons are first recruited in the song yields precisely timed multiple sequences of bursts throughout the song, not the previously envisioned single sequence of bursts treated as events having statistically independent timing. A given moment in time engages multiple sequences and both single bursting and multibursting HVC X simultaneously. This suggests a model where a population of HVC X sharing common intrinsic properties driving spike rebound excitation influence the timing of a given HVC X burst through lateral inhibitory interactions. Perturbations in burst timing, representing error, could propagate in time. Our results extend the concept of central pattern generators to complex vertebrate vocal learning and suggest that network activity (timing of inhibition) and HVC X intrinsic properties become coordinated during developmental birdsong learning.

3.
Neurobiol Learn Mem ; 180: 107407, 2021 04.
Article in English | MEDLINE | ID: mdl-33631346

ABSTRACT

Although information processing and storage in the brain is thought to be primarily orchestrated by synaptic plasticity, other neural mechanisms such as intrinsic plasticity are available. While a number of recent studies have described the plasticity of intrinsic excitability in several types of neurons, the significance of non-synaptic mechanisms in memory and learning remains elusive. After reviewing plasticity of intrinsic excitation in relation to learning and homeostatic mechanisms, we focus on the intrinsic properties of a class of basal-ganglia projecting song system neurons in zebra finch, how these related to each bird's unique learned song, how these properties change over development, and how they are maintained dynamically to rapidly change in response to auditory feedback perturbations. We place these results in the broader theme of learning and changes in intrinsic properties, emphasizing the computational implications of this form of plasticity, which are distinct from synaptic plasticity. The results suggest that exploring reciprocal interactions between intrinsic and network properties will be a fruitful avenue for understanding mechanisms of birdsong learning.


Subject(s)
Brain/physiology , Finches , Music , Neural Pathways/physiology , Neuronal Plasticity/physiology , Action Potentials , Animals , Cell Membrane , High Vocal Center/physiology , Homeostasis
4.
PLoS Biol ; 18(11): e3000929, 2020 11.
Article in English | MEDLINE | ID: mdl-33201883

ABSTRACT

Birds and mammals share specialized forms of sleep including slow wave sleep (SWS) and rapid eye movement sleep (REM), raising the question of why and how specialized sleep evolved. Extensive prior studies concluded that avian sleep lacked many features characteristic of mammalian sleep, and therefore that specialized sleep must have evolved independently in birds and mammals. This has been challenged by evidence of more complex sleep in multiple songbird species. To extend this analysis beyond songbirds, we examined a species of parrot, the sister taxon to songbirds. We implanted adult budgerigars (Melopsittacus undulatus) with electroencephalogram (EEG) and electrooculogram (EOG) electrodes to evaluate sleep architecture, and video monitored birds during sleep. Sleep was scored with manual and automated techniques, including automated detection of slow waves and eye movements. This can help define a new standard for how to score sleep in birds. Budgerigars exhibited consolidated sleep, a pattern also observed in songbirds, and many mammalian species, including humans. We found that REM constituted 26.5% of total sleep, comparable to humans and an order of magnitude greater than previously reported. Although we observed no spindles, we found a clear state of intermediate sleep (IS) similar to non-REM (NREM) stage 2. Across the night, SWS decreased and REM increased, as observed in mammals and songbirds. Slow wave activity (SWA) fluctuated with a 29-min ultradian rhythm, indicating a tendency to move systematically through sleep states as observed in other species with consolidated sleep. These results are at variance with numerous older sleep studies, including for budgerigars. Here, we demonstrated that lighting conditions used in the prior budgerigar study-and commonly used in older bird studies-dramatically disrupted budgerigar sleep structure, explaining the prior results. Thus, it is likely that more complex sleep has been overlooked in a broad range of bird species. The similarities in sleep architecture observed in mammals, songbirds, and now budgerigars, alongside recent work in reptiles and basal birds, provide support for the hypothesis that a common amniote ancestor possessed the precursors that gave rise to REM and SWS at one or more loci in the parallel evolution of sleep in higher vertebrates. We discuss this hypothesis in terms of the common plan of forebrain organization shared by reptiles, birds, and mammals.


Subject(s)
Melopsittacus/physiology , Sleep/physiology , Animals , Biological Evolution , Circadian Rhythm/physiology , Electroencephalography/veterinary , Electrooculography/veterinary , Electrophysiological Phenomena , Eye Movements/physiology , Female , Humans , Male , Mammals/physiology , Photoperiod , Polysomnography/veterinary , Sleep, REM/physiology , Sleep, Slow-Wave/physiology , Species Specificity , Ultradian Rhythm/physiology
5.
Curr Biol ; 30(18): R1056-R1058, 2020 09 21.
Article in English | MEDLINE | ID: mdl-32961164

ABSTRACT

Analysis of the rhythm structure of the songs of two songbird species and corpora of human music finds compelling similarities in rhythm categories and the effects of tempo. This gives insight into the neuroethological basis of song and music production.


Subject(s)
Music , Songbirds , Animals , Auditory Perception , Humans
6.
Nat Commun ; 11(1): 952, 2020 02 19.
Article in English | MEDLINE | ID: mdl-32075972

ABSTRACT

Neurons regulate their intrinsic physiological properties, which could influence network properties and contribute to behavioral plasticity. Recording from adult zebra finch brain slices we show that within each bird basal ganglia Area X-projecting (HVCX) neurons share similar spike waveform morphology and timing of spike trains, with modeling indicating similar magnitudes of five principal ion currents. These properties vary among birds in lawful relation to acoustic similarity of the birds' songs, with adult sibling pairs (same songs) sharing similar waveforms and spiking characteristics. The properties are maintained dynamically: HVCX within juveniles learning to sing show variable properties, whereas the uniformity rapidly degrades within hours in adults singing while exposed to abnormal (delayed) auditory feedback. Thus, within individual birds the population of current magnitudes covary over the arc of development, while rapidly responding to changes in feedback (in adults). This identifies network interactions with intrinsic properties that affect information storage and processing of learned vocalizations.


Subject(s)
Finches/physiology , Learning/physiology , Neurons/physiology , Vocalization, Animal/physiology , Action Potentials , Animals , Feedback, Sensory , Finches/anatomy & histology , High Vocal Center/anatomy & histology , High Vocal Center/cytology , High Vocal Center/metabolism , Male , Models, Neurological , Nerve Net/cytology , Nerve Net/metabolism , Neuronal Plasticity
7.
Nat Commun ; 9(1): 3093, 2018 08 06.
Article in English | MEDLINE | ID: mdl-30082791

ABSTRACT

Reconsolidation theory describes memory formation as an ongoing process that cycles between labile and stable states. Though sleep is critical for the initial consolidation of a memory, there has been little evidence that sleep facilitates reconsolidation. We now demonstrate in two experiments that a sleep-consolidated memory can be destabilized if the memory is reactivated by retrieval. The destabilized memory, which can be impaired if an interference task is encountered after, but not before, the memory is reactivated, is then reconsolidated after sleep. In two additional experiments, we provide evidence suggesting that the learning of the interference task promotes the subsequent sleep-dependent enhancement of the original memory. These results provide novel insight into the complex mechanisms of memory processing, as well as critical evidence supporting the view that long-term memory formation involves a dynamic process of sleep-dependent consolidation, use-dependent destabilization, and sleep-dependent reconsolidation.


Subject(s)
Memory Consolidation , Memory , Sleep , Starlings/physiology , Vocalization, Animal , Animals , Female , Hearing , Learning , Male , Memory, Long-Term , Mental Recall , Reproducibility of Results
8.
Learn Mem ; 25(7): 325-329, 2018 07.
Article in English | MEDLINE | ID: mdl-29907640

ABSTRACT

Newly encoded, labile memories are prone to disruption during post-learning wakefulness. Here we examine the contributions of retroactive and proactive interference to daytime forgetting on an auditory classification task in a songbird. While both types of interference impair performance, they do not develop concurrently. The retroactive interference of task-B on task-A developed during the learning of task-B, whereas the proactive interference of task-A on task-B emerged during subsequent waking retention. These different time courses indicate an asymmetry in the emergence of retroactive and proactive interference and suggest a mechanistic framework for how different types of interference between new memories develop.


Subject(s)
Auditory Perception/physiology , Behavior, Animal/physiology , Inhibition, Psychological , Learning/physiology , Memory Consolidation/physiology , Wakefulness/physiology , Animals , Starlings
10.
Chaos ; 27(12): 126802, 2017 Dec.
Article in English | MEDLINE | ID: mdl-29289057

ABSTRACT

Networks of nonlinear systems contain unknown parameters and dynamical degrees of freedom that may not be observable with existing instruments. From observable state variables, we want to estimate the connectivity of a model of such a network and determine the full state of the model at the termination of a temporal observation window during which measurements transfer information to a model of the network. The model state at the termination of a measurement window acts as an initial condition for predicting the future behavior of the network. This allows the validation (or invalidation) of the model as a representation of the dynamical processes producing the observations. Once the model has been tested against new data, it may be utilized as a predictor of responses to innovative stimuli or forcing. We describe a general framework for the tasks involved in the "inverse" problem of determining properties of a model built to represent measured output from physical, biological, or other processes when the measurements are noisy, the model has errors, and the state of the model is unknown when measurements begin. This framework is called statistical data assimilation and is the best one can do in estimating model properties through the use of the conditional probability distributions of the model state variables, conditioned on observations. There is a very broad arena of applications of the methods described. These include numerical weather prediction, properties of nonlinear electrical circuitry, and determining the biophysical properties of functional networks of neurons. Illustrative examples will be given of (1) estimating the connectivity among neurons with known dynamics in a network of unknown connectivity, and (2) estimating the biophysical properties of individual neurons in vitro taken from a functional network underlying vocalization in songbirds.

11.
Biol Cybern ; 110(6): 417-434, 2016 12.
Article in English | MEDLINE | ID: mdl-27688218

ABSTRACT

With the goal of building a model of the HVC nucleus in the avian song system, we discuss in detail a model of HVC[Formula: see text] projection neurons comprised of a somatic compartment with fast Na[Formula: see text] and K[Formula: see text] currents and a dendritic compartment with slower Ca[Formula: see text] dynamics. We show this model qualitatively exhibits many observed electrophysiological behaviors. We then show in numerical procedures how one can design and analyze feasible laboratory experiments that allow the estimation of all of the many parameters and unmeasured dynamical variables, given observations of the somatic voltage [Formula: see text] alone. A key to this procedure is to initially estimate the slow dynamics associated with Ca, blocking the fast Na and K variations, and then with the Ca parameters fixed estimate the fast Na and K dynamics. This separation of time scales provides a numerically robust method for completing the full neuron model, and the efficacy of the method is tested by prediction when observations are complete. The simulation provides a framework for the slice preparation experiments and illustrates the use of data assimilation methods for the design of those experiments.


Subject(s)
Models, Neurological , Neurons , Songbirds , Animals , Dendrites
12.
Sci Rep ; 6: 32749, 2016 09 08.
Article in English | MEDLINE | ID: mdl-27605157

ABSTRACT

We report on the construction of neuron models by assimilating electrophysiological data with large-scale constrained nonlinear optimization. The method implements interior point line parameter search to determine parameters from the responses to intracellular current injections of zebra finch HVC neurons. We incorporated these parameters into a nine ionic channel conductance model to obtain completed models which we then use to predict the state of the neuron under arbitrary current stimulation. Each model was validated by successfully predicting the dynamics of the membrane potential induced by 20-50 different current protocols. The dispersion of parameters extracted from different assimilation windows was studied. Differences in constraints from current protocols, stochastic variability in neuron output, and noise behave as a residual temperature which broadens the global minimum of the objective function to an ellipsoid domain whose principal axes follow an exponentially decaying distribution. The maximum likelihood expectation of extracted parameters was found to provide an excellent approximation of the global minimum and yields highly consistent kinetics for both neurons studied. Large scale assimilation absorbs the intrinsic variability of electrophysiological data over wide assimilation windows. It builds models in an automatic manner treating all data as equal quantities and requiring minimal additional insight.


Subject(s)
Brain/physiology , Electrophysiology/methods , Models, Neurological , Animals , Bayes Theorem , Finches , Ion Channels/physiology , Male , Neurons/physiology , Reproducibility of Results
13.
J Neurophysiol ; 114(5): 2912-22, 2015 Nov.
Article in English | MEDLINE | ID: mdl-26378204

ABSTRACT

Highly coordinated learned behaviors are key to understanding neural processes integrating the body and the environment. Birdsong production is a widely studied example of such behavior in which numerous thoracic muscles control respiratory inspiration and expiration: the muscles of the syrinx control syringeal membrane tension, while upper vocal tract morphology controls resonances that modulate the vocal system output. All these muscles have to be coordinated in precise sequences to generate the elaborate vocalizations that characterize an individual's song. Previously we used a low-dimensional description of the biomechanics of birdsong production to investigate the associated neural codes, an approach that complements traditional spectrographic analysis. The prior study used algorithmic yet manual procedures to model singing behavior. In the present work, we present an automatic procedure to extract low-dimensional motor gestures that could predict vocal behavior. We recorded zebra finch songs and generated synthetic copies automatically, using a biomechanical model for the vocal apparatus and vocal tract. This dynamical model described song as a sequence of physiological parameters the birds control during singing. To validate this procedure, we recorded electrophysiological activity of the telencephalic nucleus HVC. HVC neurons were highly selective to the auditory presentation of the bird's own song (BOS) and gave similar selective responses to the automatically generated synthetic model of song (AUTO). Our results demonstrate meaningful dimensionality reduction in terms of physiological parameters that individual birds could actually control. Furthermore, this methodology can be extended to other vocal systems to study fine motor control.


Subject(s)
Animal Structures/physiology , Finches/physiology , High Vocal Center/physiology , Models, Neurological , Neurons/physiology , Pattern Recognition, Automated/methods , Vocalization, Animal/physiology , Action Potentials , Animals , Computer Simulation , Sound , Sound Spectrography , Trachea/physiology
14.
Article in English | MEDLINE | ID: mdl-26319311

ABSTRACT

Auditory feedback (AF) plays a critical role in vocal learning. Previous studies in songbirds suggest that low-frequency (<~1 kHz) components may be salient cues in AF. We explored this with auditory stimuli including the bird's own song (BOS) and BOS variants with increased relative power at low frequencies (LBOS). We recorded single units from BOS-selective neurons in two forebrain nuclei (HVC and Area X) in anesthetized zebra finches. Song-evoked responses were analyzed based on both rate (spike counts) and temporal coding of spike trains. The BOS and LBOS tended to evoke similar spike-count responses in substantially overlapping populations of neurons in both HVC and Area X. Analysis of spike patterns demonstrated temporal coding information that discriminated among the BOS and LBOS stimuli significantly better than spike counts in the majority of HVC (94 %) and Area X (85 %) neurons. HVC neurons contained more and a broader range of temporal coding information to discriminate among the stimuli than Area X neurons. These results are consistent with a role of spike timing in coding differences in the spectral components of BOS in HVC and Area X neurons.


Subject(s)
Action Potentials/physiology , Auditory Perception/physiology , Evoked Potentials, Auditory/physiology , Feedback, Sensory/physiology , Neurons, Afferent/physiology , Prosencephalon/cytology , Acoustic Stimulation , Animals , Finches , Fourier Analysis , Prosencephalon/injuries , Prosencephalon/physiology , Vocalization, Animal/physiology
15.
Science ; 349(6249): 688-9, 2015 Aug 14.
Article in English | MEDLINE | ID: mdl-26273040
16.
Sci Rep ; 5: 8800, 2015 Mar 05.
Article in English | MEDLINE | ID: mdl-25739659

ABSTRACT

Vocal control and learning are critically dependent on auditory feedback in songbirds and humans. Continuous delayed auditory feedback (cDAF) robustly disrupts speech fluency in normal humans and has ameliorative effects in some stutterers; however, evaluations of the effects of cDAF on songbirds are rare. We exposed singing young (141-151 days old) adult zebra finch males to high-amplitude cDAF. cDAF exposure was achieved by the recording of bone-conducted sounds using a piezoelectric accelerometer, which resulted in high-quality song recordings that were relatively uncontaminated by airborne sounds. Under this condition of cDAF, birds rapidly (2-6 days) changed their song syllable timing. The one bird for which we were able to maintain the accelerometer recordings over a long period of time recovered slowly over more than a month after cDAF was discontinued. These results demonstrate that cDAF can cause substantial changes in the motor program for syllable timing generation over short intervals of time in adult zebra finches.


Subject(s)
Auditory Perception , Bone Conduction , Feedback, Sensory , Songbirds/physiology , Animals , Sound , Sound Spectrography
17.
Curr Top Behav Neurosci ; 25: 207-37, 2015.
Article in English | MEDLINE | ID: mdl-25201480

ABSTRACT

How new experiences are solidified into long-lasting memories is a central question in the study of brain and behavior. One of the most intriguing discoveries in memory research is that brain activity during sleep helps to transform newly learned information and skills into robust memories. Though the first experimental work linking sleep and memory was conducted 90 years ago by Jenkins and Dallenbach, the case for sleep-dependent memory consolidation has only garnered strong support in the last decade. Recent studies in humans provide extensive behavioral, imaging, and polysomnographic data supporting sleep consolidation of a broad range of memory tasks. Likewise, studies in a few animal model systems have elucidated potential mechanisms contributing to sleep consolidation such as neural reactivation and synaptic homeostasis. Here, we present an overview of sleep-dependent memory consolidation, focusing on how investigations of sleep and learning in birds have complemented the progress made in mammalian systems by emphasizing a strong connection between behavior and physiology. We begin by describing the behavioral approach that has been utilized to demonstrate sleep consolidation in humans. We then address neural reactivation in the rodent hippocampal system as a putative mechanism of sleep consolidation. Next, we discuss the role of sleep in the learning and maintenance of song in zebra finches. We note that while both the rodent and zebra finch systems provide evidence for sleep-dependent memory changes in physiology and behavior, neither duplicates the pattern of changes most commonly observed in humans. Finally, we present a recently developed model of sleep consolidation involving auditory classification learning in European starlings , which has the potential to connect behavioral evidence of sleep consolidation as developed in humans with underlying neural mechanisms observable in animals.


Subject(s)
Behavior, Animal/physiology , Memory/physiology , Sleep/physiology , Songbirds/physiology , Animals , Humans
18.
Biol Cybern ; 108(4): 495-516, 2014 Aug.
Article in English | MEDLINE | ID: mdl-24962080

ABSTRACT

Recent results demonstrate techniques for fully quantitative, statistical inference of the dynamics of individual neurons under the Hodgkin-Huxley framework of voltage-gated conductances. Using a variational approximation, this approach has been successfully applied to simulated data from model neurons. Here, we use this method to analyze a population of real neurons recorded in a slice preparation of the zebra finch forebrain nucleus HVC. Our results demonstrate that using only 1,500 ms of voltage recorded while injecting a complex current waveform, we can estimate the values of 12 state variables and 72 parameters in a dynamical model, such that the model accurately predicts the responses of the neuron to novel injected currents. A less complex model produced consistently worse predictions, indicating that the additional currents contribute significantly to the dynamics of these neurons. Preliminary results indicate some differences in the channel complement of the models for different classes of HVC neurons, which accords with expectations from the biology. Whereas the model for each cell is incomplete (representing only the somatic compartment, and likely to be missing classes of channels that the real neurons possess), our approach opens the possibility to investigate in modeling the plausibility of additional classes of channels the cell might possess, thus improving the models over time. These results provide an important foundational basis for building biologically realistic network models, such as the one in HVC that contributes to the process of song production and developmental vocal learning in songbirds.


Subject(s)
Action Potentials/physiology , Biophysical Phenomena/physiology , Models, Neurological , Neural Conduction/physiology , Neurons/physiology , Animals , Electric Stimulation , Ion Channels/physiology , Models, Statistical , Nerve Net/physiology , Nonlinear Dynamics , Patch-Clamp Techniques , Predictive Value of Tests , Reproducibility of Results
19.
Biol Cybern ; 108(3): 261-73, 2014 Jun.
Article in English | MEDLINE | ID: mdl-24760370

ABSTRACT

Estimating the behavior of a network of neurons requires accurate models of the individual neurons along with accurate characterizations of the connections among them. Whereas for a single cell, measurements of the intracellular voltage are technically feasible and sufficient to characterize a useful model of its behavior, making sufficient numbers of simultaneous intracellular measurements to characterize even small networks is infeasible. This paper builds on prior work on single neurons to explore whether knowledge of the time of spiking of neurons in a network, once the nodes (neurons) have been characterized biophysically, can provide enough information to usefully constrain the functional architecture of the network: the existence of synaptic links among neurons and their strength. Using standardized voltage and synaptic gating variable waveforms associated with a spike, we demonstrate that the functional architecture of a small network of model neurons can be established.


Subject(s)
Computer Simulation , Models, Neurological , Nerve Net/physiology , Neurons/physiology , Action Potentials , Animals , Humans , Regression Analysis
20.
J Neurosci ; 33(27): 11136-44, 2013 Jul 03.
Article in English | MEDLINE | ID: mdl-23825417

ABSTRACT

In most animals that vocalize, control of fundamental frequency is a key element for effective communication. In humans, subglottal pressure controls vocal intensity but also influences fundamental frequency during phonation. Given the underlying similarities in the biomechanical mechanisms of vocalization in humans and songbirds, songbirds offer an attractive opportunity to study frequency modulation by pressure. Here, we present a novel technique for dynamic control of subsyringeal pressure in zebra finches. By regulating the opening of a custom-built fast valve connected to the air sac system, we achieved partial or total silencing of specific syllables, and could modify syllabic acoustics through more complex manipulations of air sac pressure. We also observed that more nuanced pressure variations over a limited interval during production of a syllable concomitantly affected the frequency of that syllable segment. These results can be explained in terms of a mathematical model for phonation that incorporates a nonlinear description for the vocal source capable of generating the observed frequency modulations induced by pressure variations. We conclude that the observed interaction between pressure and frequency was a feature of the source, not a result of feedback control. Our results indicate that, beyond regulating phonation or its absence, regulation of pressure is important for control of fundamental frequencies of vocalizations. Thus, although there are separate brainstem pathways for syringeal and respiratory control of song production, both can affect airflow and frequency. We hypothesize that the control of pressure and frequency is combined holistically at higher levels of the vocalization pathways.


Subject(s)
Air Sacs/physiology , Phonation/physiology , Songbirds/physiology , Vocalization, Animal/physiology , Animals , Finches , Humans , Male , Models, Neurological
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