Periodotopy in the gerbil inferior colliculus: local clustering rather than a gradient map

Periodicities in sound waveforms are widespread, and shape important perceptual attributes of sound including rhythm and pitch. Previous studies have indicated that, in the inferior colliculus (IC), a key processing stage in the auditory midbrain, neurons tuned to different periodicities might be arranged along a periodotopic axis which runs approximately orthogonal to the tonotopic axis. Here we map out the topography of frequency and periodicity tuning in the IC of gerbils in unprecedented detail, using pure tones and different periodic sounds, including click trains, sinusoidally amplitude modulated (SAM) noise and iterated rippled noise. We found that while the tonotopic map exhibited a clear and highly reproducible gradient across all animals, periodotopic maps varied greatly across different types of periodic sound and from animal to animal. Furthermore, periodotopic gradients typically explained only about 10% of the variance in modulation tuning between recording sites. However, there was a strong local clustering of periodicity tuning at a spatial scale of ca. 0.5 mm, which also differed from animal to animal.

• Publication year

  2015

• Venue

  Front. Neural Circuits

• Publication date

  2015-08-04

• Fields of study

  Biology, Medicine, Physics

• Identifiers
  DOI 10.3389/fncir.2015.00037PMID 26379508PMCID 4550179
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The Neural Code for Auditory Space Depends on Sound Frequency and Head Size in an Optimal Manner

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• Patterns of convergence in the central nucleus of the inferior colliculus of the Mongolian gerbil: organization of inputs from the superior olivary complex in the low frequency representation

  2013cited by this paper
• Proportional spike-timing precision and firing reliability underlie efficient temporal processing of periodicity and envelope shape cues.

  2013cited by this paper
• Spectrotemporal sound preferences of neighboring inferior colliculus neurons: implications for local circuitry and processing

  2012cited by this paper
• Orthogonal representation of sound dimensions in the primate midbrain

  2011influential reference
• Multiplexed and Robust Representations of Sound Features in Auditory Cortex

  2011cited by this paper
• Quantifying Time-Varying Multiunit Neural Activity Using Entropy-Based Measures

  2010cited by this paper
• Spectral and temporal modulation tradeoff in the inferior colliculus.

  2010cited by this paper
• Selective Electrical Stimulation of the Auditory Nerve Activates a Pathway Specialized for High Temporal Acuity

  2010cited by this paper
• Neural Modulation Tuning Characteristics Scale to Efficiently Encode Natural Sound Statistics

  2010cited by this paper
• On pitch, the ear and the brain of the beholder. Focus on "neural coding of periodicity in marmoset auditory cortex.".

  2010cited by this paper
• The Modulation Transfer Function for Speech Intelligibility

  2009cited by this paper
• Intracellular responses of neurons in the mouse inferior colliculus to sinusoidal amplitude-modulated tones.

  2009cited by this paper
• Interdependent Encoding of Pitch, Timbre, and Spatial Location in Auditory Cortex

  2009cited by this paper
• A computational model of human auditory signal processing and perception.

  2008cited by this paper
• Distinct Roles for Onset and Sustained Activity in the Neuronal Code for Temporal Periodicity and Acoustic Envelope Shape

  2008cited by this paper
• The representation of amplitude modulations in the mammalian auditory midbrain.

  2008cited by this paper
• Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Injections, Tones of Different Durations, and Sinusoidal Amplitude-modulated Tones Comparison of Responses of Neurons in the Mouse Inferior Colliculus to Current Cortex Conductive Hearing Loss Disrupts Synaptic and Spi

  2008cited by this paper
• A Discontinuous Tonotopic Organization in the Inferior Colliculus of the Rat

  2008cited by this paper
• Response properties of neighboring neurons in the auditory midbrain for pure-tone stimulation: a tetrode study.

  2007cited by this paper
• Tuning to sound frequency in auditory field potentials.

  2007cited by this paper
• The auditory midbrain implant: a new auditory prosthesis for neural deafness-concept and device description.

  2006cited by this paper
• Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds

  2005cited by this paper
• Duration selectivity of neurons in the inferior colliculus of the big brown bat: tolerance to changes in sound level.

  2005cited by this paper
• An atlas of the inferior colliculus of the gerbil in three dimensions.

  2005influential reference
• Neural processing of amplitude-modulated sounds.

  2004cited by this paper
• Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex.

  2002cited by this paper
• Nonlinear Spectrotemporal Sound Analysis by Neurons in the Auditory Midbrain

  2002cited by this paper
• Temporal and spatial coding of periodicity information in the inferior colliculus of awake chinchilla (Chinchilla laniger).

  2002cited by this paper
• Subcortical neural coding mechanisms for auditory temporal processing.

  2001cited by this paper
• Temporal representation of iterated rippled noise as a function of delay and sound level in the ventral cochlear nucleus.

  2001cited by this paper
• The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex

  2001cited by this paper
• Interdependence of spatial and temporal coding in the auditory midbrain.

  2000cited by this paper
• Duration tuning in the mouse auditory midbrain.

  2000cited by this paper
• Influence of experience on orientation maps in cat visual cortex

  1999cited by this paper
• A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque.

  1998cited by this paper
• Laminar fine structure of frequency organization in auditory midbrain

  1997cited by this paper
• Preservation of amplitude modulation coding in the presence of background noise by chinchilla auditory-nerve fibers.

  1996cited by this paper
• Time-domain modeling of peripheral auditory processing: a modular architecture and a software platform.

  1995cited by this paper
• Neural encoding of amplitude modulation within the auditory midbrain of squirrel monkeys.

  1994cited by this paper
• Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus.

  1994cited by this paper
• Responses of neurons in the ferret superior colliculus to the spatial location of tonal stimuli.

  1994cited by this paper
• Development of orientation selectivity in ferret visual cortex and effects of deprivation

  1993cited by this paper
• Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement.

  1990cited by this paper
• Encoding of amplitude modulation in the gerbil cochlear nucleus: II. Possible neural mechanisms.

  1990cited by this paper
• Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise.

  1989cited by this paper
• Periodicity coding in the inferior colliculus of the cat. II. Topographical organization.

  1988influential reference
• Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms.

  1988influential reference
• Modulation transfer function

  1987cited by this paper
• Signal processing technique to extract neuronal activity from noise.

  1987cited by this paper
• Tone-threshold mapping in the inferior colliculus of the house mouse.

  1986cited by this paper
• Inferior colliculus of the house mouse. I. A quantitative study of tonotopic organization, frequency representation, and tone‐threshold distribution

  1985cited by this paper
• Tonotopic organization in the central auditory pathway of the mongolian gerbil: A 2‐deoxyglucose study

  1982cited by this paper
• Representation of the cochlea within the inferior colliculus of the cat.

  1974cited by this paper
• Tonotopic organization: review and analysis.

  1974cited by this paper
• Some discharge characteristics of single neurons in the inferior colliculus of the cat. II. Timing of the discharges and observations on binaural stimulation.

  1963cited by this paper

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• Neural processing and perception of Schroeder‐phase harmonic tone complexes in the gerbil: Relating single‐unit neurophysiology to behavior

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• The precedence effect in spatial hearing manifests in cortical neural population responses

  2022cites this paper
• Reduction in sound discrimination in noise is related to envelope similarity and not to a decrease in envelope tracking abilities

  2022cites this paper
• Neural Decoding of Inferior Colliculus Multiunit Activity for Sound Category identification with temporal correlation and deep learning

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  2022cites this paper
• Neurometric correlates to sensitive high-frequency sound amplitude modulation detection by mice

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  2021cites this paper
• Sensitivity to interaural time differences in the inferior colliculus of cochlear implanted rats with or without hearing experience.

  2021cites this paper
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  2019influential citation
• Near physiological spectral selectivity of cochlear optogenetics

  2019cites this paper
• Contrast gain control in mouse auditory cortex

  2018influential citation
• Microsecond Interaural Time Difference Discrimination Restored by Cochlear Implants After Neonatal Deafness

  2018cites this paper
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  2018influential citation
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