Local versus global scales of organization in auditory cortex

doi:10.1016/j.tins.2014.06.003

Trends in Neurosciences

Volume 37, Issue 9, September 2014, Pages 502-510

https://doi.org/10.1016/j.tins.2014.06.003 Get rights and content

Highlights

•
Topographic organization is a hallmark of sensory cortical organization.
•
Topography of sound frequency, tonotopy, in auditory cortex is robust at large spatial scales ranging from hundreds of microns to centimeters.
•
Tonotopy is not robust at the level of neighboring neurons or subcellular compartments within a neuron.
•
Auditory cortical circuitry can simultaneously support globally systematic, yet locally heterogeneous representations of fundamental sound properties.

Topographic organization is a hallmark of sensory cortical organization. Topography is robust at spatial scales ranging from hundreds of microns to centimeters, but can dissolve at the level of neighboring neurons or subcellular compartments within a neuron. This dichotomous spatial organization is especially pronounced in the mouse auditory cortex, where an orderly tonotopic map can arise from heterogeneous frequency tuning between local neurons. Here, we address a debate surrounding the robustness of tonotopic organization in the auditory cortex that has persisted in some form for over 40 years. Drawing from various cortical areas, cortical layers, recording methodologies, and species, we describe how auditory cortical circuitry can simultaneously support a globally systematic, yet locally heterogeneous representation of this fundamental sound property.

Section snippets

A history of progress and controversy

The first evidence for a spatially organized representation of sound frequency at the level of the cerebral cortex (see Glossary) came from 19th century lesion experiments in dogs, in which specific behavioral deficits in discriminating low, middle, or high pitch sounds were attributed to the location of focal ablations along the posterior–anterior extent of perisylvian cortex 1, 2. A neurophysiological demonstration of cochleotopy was provided decades later by recording evoked potentials from

General principles of auditory cortex organization

Primary auditory areas are distinguished from secondary areas according to three criteria. First, they receive heavy input from the lemniscal, tonotopically organized subdivision of the auditory thalamus, named the ventral subdivision of the medial geniculate body (MGBv) based on its anatomical location in cats; second, they exhibit anatomical or neurochemical features consistent with primary sensory cortex such as koniocellular cytoarchitecture, dense myelination, and elevated expression

Low resolution optical imaging reveals tonotopic order

Imaging methods (Box 1) make it possible to visualize correlates of neural activity, such as hemodynamic responses, over large areas (many mm²) of the brain and thus enable the investigation of the functional representation of relevant stimulus features.

Compared with the successful application of intrinsic signal imaging in the visual cortex, its successful application in the auditory cortex has proven more difficult possibly owing to the poor driven rates in superficial layers of the auditory

The case of the mouse

Compared with humans, the hearing range of the mouse is significantly higher and nearly half as wide (in octaves: approximately 3 kHz to 100 kHz, approximately 5 octaves as compared to 20 Hz to 16 kHz, approximately 10 octaves). Despite these differences, the mouse is becoming an increasingly popular model for studies of the auditory cortex. Many of the newer imaging and optogenetic techniques have been pioneered in the mouse, and the availability of genetically modified mouse strains makes it

High resolution imaging: beyond smooth tonotopy

Although the results surveyed up to this point seem to have settled the issue of the existence of a tonotopic map in the auditory cortex, the picture has been muddled again when Ca²⁺ indicators such as Oregon Green Bapta-1 (OGB-1) have been introduced into neurons in live animals and in vivo Ca²⁺ signals have been measured with two-photon imaging 60, 61, 62, 63 (Box 1). The Ca²⁺ signals are due to voltage-activated currents, and when measured from neuronal somata they reflect action potentials

Comparing different methodologies

Which picture of the tonotopic organization of auditory cortex is the valid one? Is it the smooth tonotopic organization that emerges from low resolution imaging and microelectrode mapping or is it the heterogeneous organization that emerges from two-photon imaging? Or may both pictures be different approximations to the same reality?

Many of the differences between the different methodologies are probably due to increased spatial resolution of two-photon imaging over electrophysiological

The olive branch

Because of these methodological issues, we currently favor a view that integrates both sets of results into a common framework. This framework should be considered as a working hypothesis to guide and be refined by future experiments. In this framework, tonotopy is the major organizational principle of the input to A1, even in mice.

There is clear evidence for a tonotopically organized forebrain region in mammals and birds, in which the auditory transduction organ converts sound frequency into a

Lessons to other sensory systems

The rapidly increasing information about fine structure of the representations in a number of sensory cortices suggests that all sensory cortices share many similarities, but also show significant differences. Studies in mouse V1 showed that although retinotopy was rather robust on large scales, it was heterogeneous on small scales [85]. This heterogeneity with respect to the organization of the periphery receptor might be an organizing feature of at least mouse layer 2/3 [86]. Nevertheless,

Lessons to other species

Much of the tonotopy controversy in its most recent reincarnation was centered around the mouse model of auditory cortex. It could be that the small brain size of mice does not support homogeneous organization by sensory maps. Although the cortical micro-organization of small carnivores has not been examined, both small and large rodents lack orientation maps in V1 62, 89, suggesting that rodents and carnivores might have evolved different cortical processing strategies. However, local

Concluding remarks

As spatial resolution of experimental techniques allow us to observe more neurons in small areas of the brain, a level of heterogeneity becomes obvious that has not been appreciated with traditional low resolution techniques. Although the smooth cortical organization uncovered at low resolution scales has provided an essential framework for understanding the organization and plasticity of primary sensory cortex, dynamic interactions between local cortical assemblies await discovery with

Acknowledgments

P.O.K. is supported by National Institutes of Health (NIH) R01DC009607. D.B.P. is supported by NIH R01DC009836. I.N. is supported by grants from the Israel Science Foundation (ISF), the US–Israel Binational Science Foundation (BSF), and the European Research Council (ERC Grant Agreement RATLAND-340063).

Glossary

Cortex: the cortex (latin ‘bark’, ‘rind’) is the thin (approximately 1–2 mm thick) layer of neurons that cover the mammalian forebrain. Most of the cortex, including auditory cortex, is composed of multiple layers (up to six) with different cellular morphology and connections. Cortical layers are grouped into the middle layer (the main thalamorecipient layer; often also called layer 4) that separates the supragranular and infragranular layers (above and below the thalamorecipient layer). The

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Trends in Neurosciences

ReviewLocal versus global scales of organization in auditory cortex

Highlights

Section snippets

A history of progress and controversy

General principles of auditory cortex organization

Low resolution optical imaging reveals tonotopic order

The case of the mouse

High resolution imaging: beyond smooth tonotopy

Comparing different methodologies

The olive branch

Lessons to other sensory systems

Lessons to other species

Concluding remarks

Acknowledgments

Glossary

Brain Res.

Hear. Res.

Brain Res.

Brain Res.

Brain Res.

Neuron

Exp. Neurol.

Neurosci. Lett.

Neuroimage

Hear. Res.

Neurosci. Res.

Neurosci. Res.

Neuroscience

J. Neurosci. Methods

Neuron

Neuron

Neuron

Curr. Opin. Neurobiol.

Ueber die musikalischen Centren des Geirns

Pflugers Arch.

Über die Funktionen der Grosshirnrinde

Topical projection of nerve fibers from local regions of the cochlea to the cerebral cortex of the cat

Bull. Johns Hopkins Hosp.

Single unit activity in the auditory cortex of the cat

Bull. Johns Hopkins Hosp.

The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical fields of the cat

J. Comp. Neurol.

Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat

J. Comp. Neurol.

Organization of auditory cortex in the owl monkey (Aotus trivirgatus)

J. Comp. Neurol.

Representation of cochlea within primary auditory cortex in the cat

J. Neurophysiol.

Tonotopic organization in auditory cortex of the cat

J. Comp. Neurol.

Classification of unit responses in the auditory cortex of the unanaesthetized and unrestrained cat

J. Physiol.

Functional architecture in cat primary auditory cortex: tonotopic organization

J. Neurophysiol.

Attention units in the auditory cortex

Science

Organization of the mammalian thalamus and its relationships to the cerebral cortex

Electroencephalogr. Clin. Neurophysiol.

The relations of thalamic connections, cellular structure and evocable electrical activity in the auditory region of the cat

J. Comp. Neurol.

The evolution of auditory cortex: the core areas

Quantitative analysis and two-dimensional reconstruction of the tonotopic organization of the auditory field L in the chick from 2-deoxyglucose data

Exp. Brain Res.

Feature extraction and tonotopic organization in the avian auditory forebrain

Exp. Brain Res.

Functional architecture in cat primary auditory cortex: columnar organization and organization according to depth

J. Neurophysiol.

Primary cortical representation of sounds by the coordination of action-potential timing

Nature

Robustness of cortical topography across fields, laminae, anesthetic states, and neurophysiological signal types

J. Neurosci.

Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex

Nature

Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex

Cereb. Cortex

Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique

Nature

Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [14C]deoxyglucose technique

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

Review
Local versus global scales of organization in auditory cortex

Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [¹⁴C]deoxyglucose technique