skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Experience-Dependent Intrinsic Plasticity During Auditory Learning
Song learning in zebra finches (Taeniopygia guttata) requires exposure to the song of a tutor, resulting in an auditory memory. This memory is the foundation for later sensorimotor learning, resulting in the production of a copy of the tutor's song. The cortical premotor nucleus HVC (proper name) is necessary for auditory and sensorimotor learning as well as the eventual production of adult song. We recently discovered that the intrinsic physiology of HVC neurons changes across stages of song learning, but are those changes the result of learning or are they experience-independent developmental changes? To test the role of auditory experience in driving intrinsic changes, patch-clamp experiments were performed comparing HVC neurons in juvenile birds with varying amounts of tutor exposure. The intrinsic physiology of HVC neurons changed as a function of tutor exposure. Counterintuitively, tutor deprivation resulted in juvenile HVC neurons showing an adult-like phenotype not present in tutor-exposed juveniles. Biophysical models were developed to predict which ion channels were modulated by experience. The models indicate that tutor exposure transiently suppressed the Ih and T-type Ca2+ currents in HVC neurons that target the basal ganglia, whereas tutor exposure increased the resting membrane potential and decreased the spike amplitude in HVC neurons that drive singing. Our findings suggest that intrinsic plasticity may be part of the mechanism for auditory learning in the HVC. More broadly, models of learning and memory should consider intrinsic plasticity as a possible mechanism by which the nervous system encodes the lasting effects of experience.  more » « less
Award ID(s):
1656360
PAR ID:
10087588
Author(s) / Creator(s):
Date Published:
Journal Name:
The Journal of neuroscience
Volume:
39
Issue:
7
ISSN:
0270-6474
Page Range / eLocation ID:
1206-1221
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Graham, Lyle J. (Ed.)
    Neurons exhibit diverse intrinsic dynamics, which govern how they integrate synaptic inputs to produce spikes. Intrinsic dynamics are often plastic during development and learning, but the effects of these changes on stimulus encoding properties are not well known. To examine this relationship, we simulated auditory responses to zebra finch song using a linear-dynamical cascade model, which combines a linear spectrotemporal receptive field with a dynamical, conductance-based neuron model, then used generalized linear models to estimate encoding properties from the resulting spike trains. We focused on the effects of a low-threshold potassium current (K LT ) that is present in a subset of cells in the zebra finch caudal mesopallium and is affected by early auditory experience. We found that K LT affects both spike adaptation and the temporal filtering properties of the receptive field. The direction of the effects depended on the temporal modulation tuning of the linear (input) stage of the cascade model, indicating a strongly nonlinear relationship. These results suggest that small changes in intrinsic dynamics in tandem with differences in synaptic connectivity can have dramatic effects on the tuning of auditory neurons. 
    more » « less
  2. Sensory experience during development has lasting effects on perception and neural processing. Exposing juvenile animals to artificial stimuli influences the tuning and functional organization of the auditory cortex, but less is known about how the rich acoustical environments experienced by vocal communicators affect the processing of complex vocalizations. Here, we show that in zebra finches (Taeniopygia guttata), a colonial-breeding songbird species, exposure to a naturalistic social-acoustical environment during development has a profound impact on auditory perceptual behavior and on cortical-level auditory responses to conspecific song. Compared to birds raised by pairs in acoustic isolation, male and female birds raised in a breeding colony were better in an operant discrimination task at recognizing conspecific songs with and without masking colony noise. Neurons in colony-reared birds had higher average firing rates, selectivity, and discriminability, especially in the narrow-spiking, putatively inhibitory neurons of a higher-order auditory area, the caudomedial nidopallium (NCM). Neurons in colony-reared birds were also less correlated in their tuning, more efficient at encoding the spectrotemporal structure of conspecific song, and better at filtering out masking noise. These results suggest that the auditory cortex adapts to noisy, complex acoustical environments by strengthening inhibitory circuitry, functionally decoupling excitatory neurons while maintaining overall excitatory-inhibitory balance. 
    more » « less
  3. Abstract Vocal learning in songbirds is mediated by cortico‐basal ganglia circuits that govern diverse functions during different stages of development. We investigated developmental changes in axonal projections to and from motor cortical regions that underlie learned vocal behavior in juvenile zebra finches (Taeniopygia guttata). Neurons in LMAN‐core project to RA, a motor cortical region that drives vocal output; these RA‐projecting neurons send a transient collateral projection to AId, a region adjacent to RA, during early vocal development. Both RA and AId project to a region of dorsal thalamus (DLM), which forms a feedback pathway to cortico‐basal ganglia circuitry. These projections provide pathways conveying efference copy and a means by which information about vocal motor output could be reintegrated into cortico‐basal ganglia circuitry, potentially aiding in the refinement of juvenile vocalizations during learning. We used tract‐tracing techniques to label the projections of LMAN‐core to AId and of RA to DLM in juvenile songbirds. The volume and density of terminal label in the LMAN‐core→AId projection declined substantially during early stages of sensorimotor learning. In contrast, the RA→DLM projection showed no developmental change. The retraction of LMAN‐core→AId axon collaterals indicates a loss of efference copy to AId and suggests that projections that are present only during early stages of sensorimotor learning mediate unique, temporally restricted processes of goal‐directed learning. Conversely, the persistence of the RA→DLM projection may serve to convey motor information forward to the thalamus to facilitate song production during both learning and maintenance of vocalizations. 
    more » « less
  4. Machado, Pedro (Ed.)
    This study emulates associative learning in rodents by using a neuromorphic robot navigating an open-field arena. The goal is to investigate how biologically inspired neural models can reproduce animal-like learning behaviors in real-world robotic systems. We constructed a neuromorphic robot by deploying computational models of spatial and sensory neurons onto a mobile platform. Different coding schemes—rate coding for vibration signals and population coding for visual signals—were implemented. The associative learning model employs 19 spiking neurons and follows Hebbian plasticity principles to associate visual cues with favorable or unfavorable locations. Our robot successfully replicated classical rodent associative learning behavior by memorizing causal relationships between environmental cues and spatial outcomes. The robot’s self-learning capability emerged from repeated exposure and synaptic weight adaptation, without the need for labeled training data. Experiments confirmed functional learning behavior across multiple trials. This work provides a novel embodied platform for memory and learning research beyond traditional animal models. By embedding biologically inspired learning mechanisms into a real robot, we demonstrate how spatial memory can be formed and expressed through sensorimotor interactions. The model’s compact structure (19 neurons) illustrates a minimal yet functional learning network, and the study outlines principles for synaptic weight and threshold design, guiding future development of more complex neuromorphic systems. 
    more » « less
  5. Abstract Synaptic and neural properties can change during periods of auditory deprivation. These changes may disrupt the computations that neurons perform. In the brainstem of chickens, auditory deprivation can lead to changes in the size and biophysics of the axon initial segment (AIS) of neurons in the sound source localization circuit. This is the phenomenon of axon initial segment (AIS) plasticity. Individuals who use cochlear implants (CIs) experience periods of hearing loss, and so we ask whether AIS plasticity in neurons of the medial superior olive (MSO), a key stage of sound location processing, would impact time difference sensitivity in the scenario of hearing with cochlear implants. The biophysical changes that we implement in our model of AIS plasticity include enlargement of the AIS and replacement of low-threshold potassium conductance with the more slowly-activated M-type potassium conductance. AIS plasticity has been observed to have a homeostatic effect with respect to excitability. In our model, AIS plasticity has the additional effect of converting MSO neurons from phasic firing type to tonic firing type. Phasic firing is known to have greater temporal sensitivity to coincident inputs. Consistent with this, we find AIS plasticity degrades time difference sensitivity in the auditory deprived MSO neuron model across a range of stimulus parameters. Our study illustrates a possible mechanism of cellular plasticity in a non-peripheral stage of neural processing that could impose barriers to sound source localization by bilateral cochlear implant users. 
    more » « less