Circuit asymmetries underlie functional lateralization in the mouse auditory cortex

Levy, Robert B.; Marquarding, Tiemo; Reid, Ashlan P.; Pun, Christopher M.; Renier, Nicolas; Oviedo, Hysell V.

doi:10.1038/s41467-019-10690-3

Cited by 50 publications

(54 citation statements)

References 46 publications

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“…Lateralization of sustained attention toward the right PPC has been 3 supported by great deal of evidence from lesion and functional imaging studies in humans (Petersen and 4 Posner, 2012;Posner and Petersen, 1990); however, the dominance of the right PPC for sustained 5 attention in rodents, to our knowledge, has not previously been recognized. Our findings are consistent 6 with prior studies showing lateralization of other higher-order cortical function in mice as seen in 7 humans (Duboc et al, 2015), including right hippocampal dominance for visuospatial memory 8 (Shinohara et al, 2012) and left hemispheric dominance for vocalization expression and response 9 (Doran et al, 2015;Ehret, 1987;Levy et al, 2019). Altogether, our results join a growing body of data 10 positioning mice as a potential translational model of some higher order cognitive functions.…”

Section: Lateralization Of Sustained Attention To the Right Posteriorsupporting

confidence: 87%

“…These findings suggest that more difficult or complex tasks may recruit the left 19 hemisphere to assist in sustaining attention. Similarly, within the auditory cortex, the right hemisphere 20 is activated by more generic tones, but the left hemisphere becomes activated by more complex 21 vocalizations (Levy et al, 2019). 22…”

Section: Positive Correlation Of Right Posterior Parietal Tg-pac and mentioning

confidence: 99%

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Right lateralized posterior parietal theta-gamma coupling during sustained attention in mice

Yang

Dunbar

Sonesra

et al. 2020

Preprint

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1Sustained attention is supported by circuits in the frontoparietal attention network. In human 2 and primate studies, the right posterior parietal cortex (PPC) shows dominance for sustained attention, 3 and phase-amplitude coupling (PAC) throughout the frontoparietal network correlates with 4 performance on attention tasks. Here we evaluate oscillatory dynamics of bilateral PPC in mice during 5 the 5-Choice Serial Reaction Time Task (5-CSRTT). Right PPC theta-gamma PAC (TG-PAC) and gamma 6 power were independently elevated to a greater degree than the left PPC during the period prior to a 7 correct response and were significantly correlated with accuracy in both simple and difficult tasks. 8Greater task difficulty was also associated with greater hemispheric asymmetry in TG-PAC, favoring the 9 right PPC. These findings highlight the engagement of PPC with sustained attention in mice, reflected by 10 increases in TG-PAC and gamma power, with maximal expression in the right hemisphere. 11 12

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Section: Lateralization Of Sustained Attention To the Right Posteriorsupporting

confidence: 87%

Section: Positive Correlation Of Right Posterior Parietal Tg-pac and mentioning

confidence: 99%

Right lateralized posterior parietal theta-gamma coupling during sustained attention in mice

Yang

Dunbar

Sonesra

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…Lateralized language processing in humans has been known for over a century (Broca, 1861;Long et al, 2016) and is crucial for normal function (Oertel et al, 2010;Cardinale et al, 2013). This division of labor has also been observed in other species including rodents (Ehret, 1987;Marlin et al, 2015), and in a recent study we began to elucidate the circuit mechanisms that could underlie lateralization by comparing the connectivity of the left and right A1 (Levy et al, 2019). We found significant hemispheric differences in the connectivity of L3 pyramidal cells in the mouse A1.…”

Section: Circuit Foundation Of Parallel Processing Between the Hemispmentioning

confidence: 53%

“…Given the limitations of experimental work in humans, we can more thoroughly interrogate potential circuit mechanisms in animal models that utilize social calls (e.g., birds and rodents). Circuit-mapping studies in the rodent A1 have begun to reveal connectivity schemes consistent with phoneme detection (Oviedo et al, 2010;Levy et al, 2019). Social calls are spectrotemporally complex, requiring neurons to integrate across frequency channels.…”

Section: Circuit Foundation Of Phoneme Detectionmentioning

confidence: 99%

“…Similarly, unnatural auditory experiences due to disease in early human infancy lead to degraded language abilities (Centers for Disease and Prevention, 2010). The implication of these findings is that exposure to the statistical structure of social calls provides the training signals that guide connectivity (Rauschecker, 1999;Levy et al, 2019). During critical periods, the brain relies on the statistical regularities of the auditory world (some sound sequences are more probable than others) to shape neural circuits in order to make detection and decoding of ethologically relevant signals faster in the future.…”

Section: Introductionmentioning

confidence: 99%

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Using Neural Circuit Interrogation in Rodents to Unravel Human Speech Decoding

Neophytou

Oviedo

2020

Front. Neural Circuits

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The neural circuits responsible for social communication are among the least understood in the brain. Human studies have made great progress in advancing our understanding of the global computations required for processing speech, and animal models offer the opportunity to discover evolutionarily conserved mechanisms for decoding these signals. In this review article, we describe some of the most well-established speech decoding computations from human studies and describe animal research designed to reveal potential circuit mechanisms underlying these processes. Human and animal brains must perform the challenging tasks of rapidly recognizing, categorizing, and assigning communicative importance to sounds in a noisy environment. The instructions to these functions are found in the precise connections neurons make with one another. Therefore, identifying circuit-motifs in the auditory cortices and linking them to communicative functions is pivotal. We review recent advances in human recordings that have revealed the most basic unit of speech decoded by neurons is a phoneme, and consider circuit-mapping studies in rodents that have shown potential connectivity schemes to achieve this. Finally, we discuss other potentially important processing features in humans like lateralization, sensitivity to fine temporal features, and hierarchical processing. The goal is for animal studies to investigate neurophysiological and anatomical pathways responsible for establishing behavioral phenotypes that are shared between humans and animals. This can be accomplished by establishing cell types, connectivity patterns, genetic pathways and critical periods that are relevant in the development and function of social communication.

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Communication‐related assessments in an Angelman syndrome mouse model

et al. 2020

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Introduction Angelman syndrome (AS) is a neurodevelopmental disorder characterized by motor deficits, seizures, some autistic‐like behaviors, and severe impairment of speech. A dysfunction of the maternally imprinted UBE3A gene, coupled with a functional yet silenced paternal copy, results in AS. Although studies of transgenic mouse models have revealed a great deal about neural populations and rescue timeframes for specific features of AS, these studies have largely failed to examine intermediate phenotypes that contribute to the profound communicative disabilities associated with AS. Methods Here, we use a variety of tasks, including assessments of rapid auditory processing and social communication. Expressive vocalizations were directly assessed and correlated against other core behavioral measures (motor, social, acoustic perception) to model putative influences on communication. Results AS mice displayed the characteristic phenotypes associated with Angelman syndrome (i.e., social and motor deficits), as well as marginal enhancements in rapid auditory processing ability. Our characterization of adult ultrasonic vocalizations further showed that AS mice produce fewer vocalizations and vocalized for a shorter amount of time when compared to controls. Additionally, a strong correlation between motor indices and ultrasonic vocalization output was shown, suggesting that the motor impairments in AS may contribute heavily to communication impairments. Conclusion In summary, the combination of motor deficits, social impairment, marginal rapid auditory enhancements, and altered ultrasonic vocalizations reported in a mouse model of AS clearly parallel the human symptoms of the disorder. This mouse model offers a novel route to interrogate the underlying genetic, physiologic, and behavioral influences on the under‐studied topic of impaired communication in AS.

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Circuit asymmetries underlie functional lateralization in the mouse auditory cortex

Cited by 50 publications

References 46 publications

Right lateralized posterior parietal theta-gamma coupling during sustained attention in mice

Right lateralized posterior parietal theta-gamma coupling during sustained attention in mice

Using Neural Circuit Interrogation in Rodents to Unravel Human Speech Decoding

Communication‐related assessments in an Angelman syndrome mouse model

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