Literature DB >> 29364073

Amplitude modulation coding in awake mice and squirrel monkeys.

Nerissa E G Hoglen1,2,3,4,5,6, Phillip Larimer1,3,7, Elizabeth A K Phillips1,2,3,6, Brian J Malone2,3,4, Andrea R Hasenstaub1,2,3,4.   

Abstract

Both mice and primates are used to model the human auditory system. The primate order possesses unique cortical specializations that govern auditory processing. Given the power of molecular and genetic tools available in the mouse model, it is essential to understand the similarities and differences in auditory cortical processing between mice and primates. To address this issue, we directly compared temporal encoding properties of neurons in the auditory cortex of awake mice and awake squirrel monkeys (SQMs). Stimuli were drawn from a sinusoidal amplitude modulation (SAM) paradigm, which has been used previously both to characterize temporal precision and to model the envelopes of natural sounds. Neural responses were analyzed with linear template-based decoders. In both species, spike timing information supported better modulation frequency discrimination than rate information, and multiunit responses generally supported more accurate discrimination than single-unit responses from the same site. However, cortical responses in SQMs supported better discrimination overall, reflecting superior temporal precision and greater rate modulation relative to the spontaneous baseline and suggesting that spiking activity in mouse cortex was less strictly regimented by incoming acoustic information. The quantitative differences we observed between SQM and mouse cortex support the idea that SQMs offer advantages for modeling precise responses to fast envelope dynamics relevant to human auditory processing. Nevertheless, our results indicate that cortical temporal processing is qualitatively similar in mice and SQMs and thus recommend the mouse model for mechanistic questions, such as development and circuit function, where its substantial methodological advantages can be exploited. NEW & NOTEWORTHY To understand the advantages of different model organisms, it is necessary to directly compare sensory responses across species. Contrasting temporal processing in auditory cortex of awake squirrel monkeys and mice, with parametrically matched amplitude-modulated tone stimuli, reveals a similar role of timing information in stimulus encoding. However, disparities in response precision and strength suggest that anatomical and biophysical differences between squirrel monkeys and mice produce quantitative but not qualitative differences in processing strategy.

Entities:  

Keywords:  amplitude modulation; auditory cortex; species comparison; temporal processing

Mesh:

Year:  2018        PMID: 29364073      PMCID: PMC6008086          DOI: 10.1152/jn.00101.2017

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  55 in total

1.  Functional organization of squirrel monkey primary auditory cortex: responses to pure tones.

Authors:  S W Cheung; P H Bedenbaugh; S S Nagarajan; C E Schreiner
Journal:  J Neurophysiol       Date:  2001-04       Impact factor: 2.714

2.  Age-related alterations in the neural coding of envelope periodicities.

Authors:  Joseph P Walton; Henry Simon; Robert D Frisina
Journal:  J Neurophysiol       Date:  2002-08       Impact factor: 2.714

3.  Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations.

Authors:  Christopher DiMattina; Xiaoqin Wang
Journal:  J Neurophysiol       Date:  2005-10-05       Impact factor: 2.714

4.  Processing of twitter-call fundamental frequencies in insula and auditory cortex of squirrel monkeys.

Authors:  A Bieser
Journal:  Exp Brain Res       Date:  1998-09       Impact factor: 1.972

5.  Diverse cortical codes for scene segmentation in primate auditory cortex.

Authors:  Brian J Malone; Brian H Scott; Malcolm N Semple
Journal:  J Neurophysiol       Date:  2015-02-18       Impact factor: 2.714

6.  Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification.

Authors:  Robert W Meredith; Jan E Janečka; John Gatesy; Oliver A Ryder; Colleen A Fisher; Emma C Teeling; Alisha Goodbla; Eduardo Eizirik; Taiz L L Simão; Tanja Stadler; Daniel L Rabosky; Rodney L Honeycutt; John J Flynn; Colleen M Ingram; Cynthia Steiner; Tiffani L Williams; Terence J Robinson; Angela Burk-Herrick; Michael Westerman; Nadia A Ayoub; Mark S Springer; William J Murphy
Journal:  Science       Date:  2011-09-22       Impact factor: 47.728

7.  Speech recognition with primarily temporal cues.

Authors:  R V Shannon; F G Zeng; V Kamath; J Wygonski; M Ekelid
Journal:  Science       Date:  1995-10-13       Impact factor: 47.728

8.  Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification.

Authors:  Ganesh Vigneswaran; Alexander Kraskov; Roger N Lemon
Journal:  J Neurosci       Date:  2011-10-05       Impact factor: 6.167

9.  The modulation transfer function for speech intelligibility.

Authors:  Taffeta M Elliott; Frédéric E Theunissen
Journal:  PLoS Comput Biol       Date:  2009-03-06       Impact factor: 4.475

10.  Vocal repertoire of the squirrel monkey (Saimiri sciureus), its analysis and significance.

Authors:  P Winter; D Ploog; J Latta
Journal:  Exp Brain Res       Date:  1966       Impact factor: 1.972

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  8 in total

1.  Amplitude modulation encoding in the auditory cortex: comparisons between the primary and middle lateral belt regions.

Authors:  Jeffrey S Johnson; Mamiko Niwa; Kevin N O'Connor; Mitchell L Sutter
Journal:  J Neurophysiol       Date:  2020-10-07       Impact factor: 2.714

2.  Responses of neurons in the rostral ventrolateral medulla of conscious cats to anticipated and passive movements.

Authors:  Derek M Miller; Asmita Joshi; Emmanuel T Kambouroglos; Isaiah C Engstrom; John P Bielanin; Samuel R Wittman; Andrew A McCall; Susan M Barman; Bill J Yates
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2020-01-15       Impact factor: 3.619

3.  Best sensitivity of temporal modulation transfer functions in laboratory mice matches the amplitude modulation embedded in vocalizations.

Authors:  Huaizhen Cai; Micheal L Dent
Journal:  J Acoust Soc Am       Date:  2020-01       Impact factor: 2.482

4.  An Emergent Population Code in Primary Auditory Cortex Supports Selective Attention to Spectral and Temporal Sound Features.

Authors:  Joshua D Downer; Jessica R Verhein; Brittany C Rapone; Kevin N O'Connor; Mitchell L Sutter
Journal:  J Neurosci       Date:  2021-07-01       Impact factor: 6.709

5.  Temporally precise population coding of dynamic sounds by auditory cortex.

Authors:  Joshua D Downer; James Bigelow; Melissa J Runfeldt; Brian J Malone
Journal:  J Neurophysiol       Date:  2021-06-02       Impact factor: 2.974

6.  Movement and VIP Interneuron Activation Differentially Modulate Encoding in Mouse Auditory Cortex.

Authors:  James Bigelow; Ryan J Morrill; Jefferson Dekloe; Andrea R Hasenstaub
Journal:  eNeuro       Date:  2019-09-18

7.  Stimulus dependent transformations between synaptic and spiking receptive fields in auditory cortex.

Authors:  Kyunghee X Kim; Craig A Atencio; Christoph E Schreiner
Journal:  Nat Commun       Date:  2020-02-27       Impact factor: 14.919

8.  Audiovisual task switching rapidly modulates sound encoding in mouse auditory cortex.

Authors:  Ryan J Morrill; James Bigelow; Jefferson DeKloe; Andrea R Hasenstaub
Journal:  Elife       Date:  2022-08-18       Impact factor: 8.713

  8 in total

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