Trends in Neurosciences
ReviewLocal versus global scales of organization in auditory cortex
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
References (92)
- et al.
Representation of the cochlear partition of the superior temporal plane of the macaque monkey
Brain Res.
(1973) Information flow in the auditory cortical network
Hear. Res.
(2011)The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami
Brain Res.
(1968)- et al.
Tonotopic organization in the avian telencephalon
Brain Res.
(1976) - et al.
Note on tonotopic organization of primary auditory cortex in the cat
Brain Res.
(1975) - et al.
Synaptic mechanisms of forward suppression in rat auditory cortex
Neuron
(2005) Functional neuroanatomy of the auditory cortex studied with [2-14C] deoxyglucose
Exp. Neurol.
(1981)Autoradiographic demonstration with 2-[14C]deoxyglucose of frequency selectivity in the auditory system of cats under conditions of functional activity
Neurosci. Lett.
(1978)Three distinct auditory areas of cortex (AI, AII, and AAF) defined by optical imaging of intrinsic signals
Neuroimage
(2000)Disrupted tonotopy of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptor
Hear. Res.
(2005)
Dual compartments of the ventral division of the medial geniculate body projecting to the core region of the auditory cortex in C57BL/6 mice
Neurosci. Res.
Transcranial photo-inactivation of neural activities in the mouse auditory cortex
Neurosci. Res.
Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivo and in vitro
Neuroscience
Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy
J. Neurosci. Methods
Chronic cellular imaging of entire cortical columns in awake mice using microprisms
Neuron
Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex
Neuron
Preceding inhibition silences layer 6 neurons in auditory cortex
Neuron
Neural maps versus salt-and-pepper organization in visual cortex
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.
Suprathreshold auditory cortex activation visualized by intrinsic signal optical imaging
Cereb. Cortex
Optical imaging of cat auditory cortex cochleotopic selectivity evoked by acute electrical stimulation of a multi-channel cochlear implant
Eur. J. Neurosci.
Optical imaging of intrinsic signals in chinchilla auditory cortex
Audiol. Neurootol.
Optical and FDG mapping of frequency-specific activity in auditory cortex
Neuroreport
Cited by (74)
Hidden hearing loss: Fifteen years at a glance
2024, Hearing ResearchCortical surface plasticity promotes map remodeling and alleviates tinnitus in adult mice
2023, Progress in Neurobiology
- *
All authors contributed equally to this work.