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Meliza, C. D.

Publications and source records attributed to Meliza, C. D..

8 recordsLinked to original sources

A geniculocortical circuit model predicts functional organization underlying efficient spatial frequency coding in the mouse visual system

Neural encoding of sensory information becomes more efficient when distinct stimuli evoke uncorrelated activity patterns. Spatial frequency (SF) information becomes decorrelated early in visual processing in a manner that involves both temporal differentiation in the dorsal lateral geniculate nucleus (dLGN) and firing rate differentiation in the primary visual cortex (V1). However, the specific functional circuit configurations that enable this synergy are not fully understood. To address this gap, we developed a geniculocortical subunit model to identify functional circuit configurations capable of producing a decorrelated V1 population response. We found that decorrelation could be explained by the combined activity of two complementary circuit configurations with distinct functional organization. The first circuit was characterized by temporally organized, late-onset dLGN inputs coupled to weak and delayed intracortical inhibition, whereas the second was characterized by less temporally constrained, early-onset dLGN inputs coupled to strong and early intracortical inhibition. Eliminating SF selectivity in upstream dLGN subunits did not affect SF decorrelation in the modeled V1 population response, indicating that decorrelation tolerates weak SF selectivity and is primarily driven by temporal organization. Together, these results suggest that biologically plausible circuit configurations are likely to produce SF decorrelation in the cortex through the temporal organization of feedforward inputs and intracortical inhibition.

neuroscience↗

A complex acoustical environment is necessary for maintenance and development in the zebra finch auditory pallium

Postnatal experience is critical to auditory development in vertebrates. The zebra finch (Taeniopygia castanotis) provides a valuable model for understanding how complex social-acoustical environments influence development of the neural circuits that support perception of vocal communication signals. We previously showed that zebra finches raised in the rich acoustical environment of a breeding colony (colony-reared, CR) perform twice as well in an operant discrimination task as birds raised with only their families (pair-reared, PR), and we identified deficits in functional properties within the auditory pallium of PR birds that could explain this behavioral difference. Here, using single-unit extracellular recordings from the L3 subdivision of field L and caudomedial nidopallium (NCM) at three developmental timepoints (18-20, 30-35, and 90-110 days post hatch), we tracked how experience affects the emergence of these functional properties. Whereas CR birds showed stable single-unit response properties from fledging to adulthood alongside improvements in population-level encoding, PR birds exhibited progressive deterioration in neural function. Deficits in PR birds began emerging at 18 days for population metrics and by 30 days for single-unit properties, worsening into adulthood. These included altered spike waveforms, firing rates, selectivity, discriminability, coding efficiency, and noise invariance. Notably, these deficits occurred despite PR birds receiving normal exposure to the song of a male tutor, suggesting that learning to sing is robust enough to compensate for impaired auditory processing. Our findings demonstrate that a complex acoustical environment is necessary for both maintenance and development of the cortical-level auditory circuits that decode conspecific vocalizations.

neuroscience↗

Cortical Processing of Conspecific Vocalizations in Zebra Finches Depends on the Early Acoustical Environment

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 and 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. Significance StatementThe statistics of the sensory inputs animals experience during postnatal development shape cortical circuits and their functional properties, but most studies examining experience-dependent plasticity in the auditory system has employed artificial stimuli with limited relevance to acoustic communication. Here, we examined how the natural social-acoustical environment experienced by zebra finches, a social songbird that breeds in large colonies, influences the development of auditory perception and the underlying auditory cortical circuits. Compared to birds raised in a more impoverished environment, colony-reared birds were better at recognizing songs of other zebra finches and had higher firing rates in the avian homolog to auditory cortex, along with changes to functional connectivity that resulted in more efficient and robust coding of conspecific song.

neuroscience↗

Rapid, activity-dependent intrinsic plasticity in the developing zebra finch auditory cortex

The acoustic environment an animal experiences early in life shapes the structure and function of its auditory system. This process of experience-dependent development is thought to be primarily orchestrated by potentiation and depression of synapses, but plasticity of intrinsic voltage dynamics may also contribute. Here we show that at the peak of the critical period for song memorization, neurons in the zebra finch caudal mesopallium, a cortical-level auditory area, can rapidly change their firing dynamics. This plasticity was only observed in birds that were reared in a complex acoustic and social environment, which also caused increased expression of the low-threshold potassium channel Kv1.1 in the plasma membrane and endoplasmic reticulum. Intrinsic plasticity depended on activity, was reversed by blocking low-threshold potassium currents, and was prevented by blocking intracellular calcium signaling. Taken together, these results suggest that Kv1.1 is rapidly mobilized to the plasma membrane by activity-dependent elevation of intracellular calcium. This produces a shift in the excitability and temporal integration of CM neurons that may be permissive for auditory learning in complex acoustic environments during a crucial period for the development of vocal perception and production.

neuroscience↗

The zebra finch auditory cortex reconstructs occluded syllables in conspecific song

In the perceptual illusion known as phonemic (or auditory) restoration, listeners hear sounds occluded by short bursts of noise. The neural mechanisms that create this illusion by generating predictions of the missing information remain poorly understood. Zebra finches (Taeniopygia guttata) use song, a sequence of complex vocal elements, to communicate in noisy social environments. Here, we found that in anesthetized finches, populations of single units in the homolog of auditory cortex respond to occluded songs as if the missing elements were present. This occurs even for songs birds have never heard, but not if the context is masked or lacks species-typical syntax. These results suggest that local neural dynamics pre-attentively instantiate a general model of conspecific song that biases auditory responses to restore missing information.

neuroscience↗

Nonlinear effects of intrinsic dynamics on temporal encoding in a model of avian auditory cortex

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 (KLT) that is present in a subset of cells in the zebra finch caudal mesopallium and is affected by early auditory experience. We found that KLT 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. Author summaryExperience-dependent developmental plasticity involves changes not only to synaptic connections, but to voltage-gated currents as well. Using biophysical models, it is straightforward to predict the effects of this intrinsic plasticity on the firing patterns of individual neurons, but it remains difficult to understand the consequences for sensory coding. We investigated this in the context of the zebra finch auditory cortex, where early exposure to a complex acoustic environment causes increased expression of a low-threshold potassium current. We simulated responses to song using a detailed biophysical model and then characterized encoding properties using generalized linear models. This analysis revealed that this potassium current has strong, nonlinear effects on how the model encodes the songs temporal structure, and that the sign of these effects depend on the temporal tuning of the synaptic inputs. This nonlinearity gives intrinsic plasticity broad scope as a mechanism for developmental learning in the auditory system.

neuroscience↗

Experience- and sex-dependent intrinsic plasticity in the zebra finch auditory cortex during song memorization

Early auditory experience is critical to the development of vocal communication. Zebra finches and other songbirds have a sensitive period when young birds memorize a song to use as a model for vocal production. We found that intrinsic spiking dynamics change dramatically during this period in the caudal mesopallium, a cortical-level auditory area. Specifically, the proportion of neurons that only fire transiently at the onset of intracellular current injections increases, along with Kv1.1, a channel that facilitates transient spiking. Plasticity is greater in males and requires exposure to a complex, noisy environment. These observations indicate that intrinsic dynamics are modulated in response to the acoustic environment to support robust auditory processing during a critical phase of vocal learning.

neuroscience↗

Intrinsic dynamics enhance decodability of neurons in a model of avian auditory cortex

Birdsong is a complex vocal communication signal, and like humans, birds need to discriminate between similar sequences of sound with different meanings. The caudal mesopallium (CM) is a cortical-level auditory area implicated in song discrimination. CM neurons respond sparsely to conspecific song and are tolerant of production variability. Intracellular recordings in CM have identified a diversity of intrinsic membrane dynamics, which could contribute to the emergence of these higher-order functional properties. We investigated this hypothesis using a novel linear-dynamical cascade model that incorporated detailed biophysical dynamics to simulate auditory responses to birdsong. Neuron models that included a low-threshold potassium current present in a subset of CM neurons showed increased selectivity and coding efficiency relative to models without this current. These results demonstrate the impact of intrinsic dynamics on sensory coding and the importance of including the biophysical characteristics of neural populations in simulation studies.

neuroscience↗