Parvalbumin neurons, temporal coding, and cortical noise in complex scene analysis

Nocon, Jian Carlo; Gritton, Howard J.; James, Nicholas M.; Han, Xue; Sen, Kamal

doi:10.1101/2021.09.11.459906

Cited by 8 publications

(20 citation statements)

References 89 publications

(227 reference statements)

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“…To better understand cortical coding of complex scenes in a mouse model amenable to circuit manipulation using genetic tools, we recently utilized a cocktail party-like experimental paradigm (Maddox et al, 2012) while recording from neurons in ACx (Figure 1A) (Nocon et al, 2022). Specifically, we recorded responses to spatially distributed sound mixtures to determine how competing sound sources influence cortical coding of stimuli.…”

Section: Resultsmentioning

confidence: 99%

“…For all simulations, target stimuli consisted of two white noise tokens modulated by human speech-shaped envelopes with a sampling frequency of 195312 Hz. These same stimuli were used for previous experiments on complex scene analysis in mouse ACx (Nocon et al, 2022).…”

Section: Stimulimentioning

confidence: 99%

“…For the optogenetic condition, we inhibited PV neurons in all layers with a hyperpolarizing current of 0.03 nA. To model the elevated spontaneous firing rate observed in single unit recordings (Nocon et al, 2022), we also simulated this by increasing the mean firing rate of the Poisson-like network noise (Figure 7A).…”

Section: Model Explains Experimentally Observed Effects Of Optogeneti...mentioning

confidence: 99%

“…Although auditory cortex (ACx) is thought to contribute to such processing, the underlying cortical mechanisms remain poorly understood. In a recent study (Nocon et al, 2022), we investigated the processing of dynamic stimuli in mouse ACx, quantifying neural discriminability of dynamic sounds in ACx, and found that optogenetic suppression of parvalbumin (PV) neurons degraded discrimination performance, and specifically temporal coding, in ACx. How do PV neurons shape cortical discrimination performance and temporal coding?…”

Section: Introductionmentioning

confidence: 99%

“…Additionally, previous models have shown that the short-term synaptic plasticity (STP) profiles of inhibitory interneurons are critical for temporal context-dependent modulation (Seay et al, 2020). Here, we implemented a multi-layer cortical network model with excitatory neurons, and both onset- and offset-responding PV neurons to explain the experimental observations in (Nocon et al, 2022). The model reveals that both onset and offset-responding PV neurons, and synaptic depression from PV to excitatory synapses are critical in sculpting cortical responses to dynamic stimuli.…”

Section: Introductionmentioning

confidence: 99%

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Parvalbumin Neurons and Cortical Coding of Dynamic Stimuli: A Network Model

Nocon

Gritton

Han

et al. 2022

Preprint

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Cortical circuits feature both excitatory and inhibitory cells that underlie the encoding of dynamic sensory stimuli, e.g., speech, music, odors, and natural scenes. While previous studies have shown that inhibition plays an important role in shaping the neural code, little is known about how excitatory and inhibitory cells coordinate to enhance encoding of temporally dynamic stimuli. Recent experimental recordings in mouse auditory cortex (ACx) have shown that optogenetic suppression of parvalbumin (PV) neurons results in a decrease of neural discriminability between dynamic stimuli with speech envelope modulations. Here, we present a multilayer model of a cortical circuit that mechanistically explains these results. The model incorporates characteristic short-term synaptic plasticity (STP) profiles of excitatory and PV cells. Crucially, the model performance is based on populations of PV cells that separately respond to stimulus onsets and offsets. We reveal that by tuning the relative strengths of inhibition from onset- and offset-responding PV cells, the cortical network model captures the broad range of neural discriminability profiles in cortical single-unit data, with varying contributions from rapid firing rate modulations and spike timing. The model also replicates and explains the experimentally observed reduction in neural discrimination performance during optogenetic suppression of PV neurons. These results suggest that distinct populations of PV neurons enhance cortical discriminability of dynamic stimuli by encoding distinct temporal features, enhancing temporal coding, and reducing cortical noise.

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Section: Resultsmentioning

confidence: 99%

Section: Stimulimentioning

confidence: 99%

Section: Model Explains Experimentally Observed Effects Of Optogeneti...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Parvalbumin Neurons and Cortical Coding of Dynamic Stimuli: A Network Model

Nocon

Gritton

Han

et al. 2022

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Developmental hearing loss–induced perceptual deficits are rescued by genetic restoration of cortical inhibition

Masri,

Mowery,

Fair

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Even a transient period of hearing loss during the developmental critical period can induce long-lasting deficits in temporal and spectral perception. These perceptual deficits correlate with speech perception in humans. In gerbils, these hearing loss–induced perceptual deficits are correlated with a reduction of both ionotropic GABA A and metabotropic GABA B receptor–mediated synaptic inhibition in auditory cortex, but most research on critical period plasticity has focused on GABA A receptors. Therefore, we developed viral vectors to express proteins that would upregulate gerbil postsynaptic inhibitory receptor subunits (GABA A , Gabra1 ; GABA B , Gabbr1b ) in pyramidal neurons, and an enzyme that mediates GABA synthesis ( GAD65 ) presynaptically in parvalbumin-expressing interneurons. A transient period of developmental hearing loss during the auditory critical period significantly impaired perceptual performance on two auditory tasks: amplitude modulation depth detection and spectral modulation depth detection. We then tested the capacity of each vector to restore perceptual performance on these auditory tasks. While both GABA receptor vectors increased the amplitude of cortical inhibitory postsynaptic potentials, only viral expression of postsynaptic GABA B receptors improved perceptual thresholds to control levels. Similarly, presynaptic GAD65 expression improved perceptual performance on spectral modulation detection. These findings suggest that recovering performance on auditory perceptual tasks depends on GABA B receptor-dependent transmission at the auditory cortex parvalbumin to pyramidal synapse and point to potential therapeutic targets for developmental sensory disorders.

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A Robust, Compact and Diverse Population Code for Competing Sounds in Auditory Cortex

Nocon

Witter

Houghton

et al. 2022

Preprint

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Cortical circuits encoding sensory information consist of populations of neurons, yet how information aggregates via pooling individual cells remains poorly understood. Such pooling may be particularly important in noisy settings where single neuron encoding is degraded. One example is the cocktail party problem, with competing sounds from multiple spatial locations. How populations of neurons in auditory cortex (ACx) code competing sounds have not been previously investigated. Here, we apply a novel information theoretic approach to estimate information in populations of neurons in ACx about competing sounds from multiple spatial locations, including both summed population (SP) and labeled line (LL) codes. We find that a small subset of neurons is sufficient to nearly maximize mutual information over different spatial configurations, with the LL code outperforming the SP code, and approaching information levels attained without noise. Moreover, with a LL code, units with diverse spatial responses, including both regular and narrow-spiking units, constitute the best pool. Finally, information in the population increases with spatial separation between target and masker, in correspondence with behavioral results on spatial release from masking in human and animals. Taken together, our results reveal that a compact and diverse population of neurons in ACx provide a robust code for competing sounds from different spatial locations.

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Parvalbumin neurons, temporal coding, and cortical noise in complex scene analysis

Cited by 8 publications

References 89 publications

Parvalbumin Neurons and Cortical Coding of Dynamic Stimuli: A Network Model

Parvalbumin Neurons and Cortical Coding of Dynamic Stimuli: A Network Model

Developmental hearing loss–induced perceptual deficits are rescued by genetic restoration of cortical inhibition

A Robust, Compact and Diverse Population Code for Competing Sounds in Auditory Cortex

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