In
physiology
Physiology (; ) is the scientific study of functions and mechanisms in a living system. As a sub-discipline of biology, physiology focuses on how organisms, organ systems, individual organs, cells, and biomolecules carry out the chemical ...
, tonotopy (from Greek tono = frequency and topos = place) is the spatial arrangement of where sounds of different frequency are processed in the brain. Tones close to each other in terms of frequency are represented in
topologically neighbouring regions in the brain. Tonotopic maps are a particular case of
topographic
Topography is the study of the forms and features of land surfaces. The topography of an area may refer to the land forms and features themselves, or a description or depiction in maps.
Topography is a field of geoscience and planetary scien ...
organization, similar to
retinotopy
Retinotopy (from Greek τόπος, place) is the mapping of visual input from the retina to neurons, particularly those neurons within the visual stream. For clarity, 'retinotopy' can be replaced with 'retinal mapping', and 'retinotopic' with 'r ...
in the visual system.
Tonotopy in the auditory system begins at the
cochlea
The cochlea is the part of the inner ear involved in hearing. It is a spiral-shaped cavity in the bony labyrinth, in humans making 2.75 turns around its axis, the modiolus. A core component of the cochlea is the Organ of Corti, the sensory org ...
, the small snail-like structure in the inner ear that sends information about sound to the brain. Different regions of the
basilar membrane
The basilar membrane is a stiff structural element within the cochlea of the inner ear which separates two liquid-filled tubes that run along the coil of the cochlea, the scala media and the scala tympani. The basilar membrane moves up and down in ...
in the
organ of Corti
The organ of Corti, or spiral organ, is the receptor organ for hearing and is located in the mammalian cochlea. This highly varied strip of epithelial cells allows for transduction of auditory signals into nerve impulses' action potential. Transd ...
, the sound-sensitive portion of the cochlea, vibrate at different sinusoidal frequencies due to variations in thickness and width along the length of the membrane. Nerves that transmit information from different regions of the basilar membrane therefore encode frequency tonotopically. This tonotopy then projects through the
vestibulocochlear nerve and associated midbrain structures to the primary auditory cortex via the auditory radiation pathway.
Throughout this radiation, organization is linear with relation to placement on the organ of Corti, in accordance to the best frequency response (that is, the frequency at which that neuron is most sensitive) of each neuron. However,
binaural fusion Binaural fusion or binaural integration is a cognitive process that involves the combination of different auditory information presented binaurally, or to each ear. In humans, this process is essential in understanding speech as one ear may pick u ...
in the
superior olivary complex
The superior olivary complex (SOC) or superior olive is a collection of brainstem nuclei that functions in multiple aspects of hearing and is an important component of the ascending and descending auditory pathways of the auditory system. The SO ...
onward adds significant amounts of information encoded in the signal strength of each ganglion. Thus, the number of tonotopic maps varies between species and the degree of binaural synthesis and separation of sound intensities; in humans, six tonotopic maps have been identified in the primary auditory cortex.
History
The earliest evidence for tonotopic organization in auditory cortex was indicated by Vladimir E. Larionov in an 1899 paper entitled "On the musical centers of the brain", which suggested that lesions in an S-shaped trajectory resulted in failure to respond to tones of different frequencies. By the 1920s, cochlear anatomy had been described and the concept of tonotopicity had been introduced. At this time, Hungarian biophysicist,
Georg von Békésy
Georg von Békésy ( hu, Békésy György, ; 3 June 1899 – 13 June 1972) was a Hungarian-American biophysicist.
By using strobe photography and silver flakes as a marker, he was able to observe that the basilar membrane moves like a surface w ...
began further exploration of tonotopy in the auditory cortex. Békésy measured the cochlear traveling wave by opening up the cochlea widely and using a strobe light and microscope to visually observe the motion on a wide variety of animals including guinea pig, chicken, mouse, rat, cow, elephant, and human temporal bone. Importantly, Békésy found that different sound frequencies caused maximum wave amplitudes to occur at different places along the
basilar membrane
The basilar membrane is a stiff structural element within the cochlea of the inner ear which separates two liquid-filled tubes that run along the coil of the cochlea, the scala media and the scala tympani. The basilar membrane moves up and down in ...
along the coil of the cochlea, which is the fundamental principal of tonotopy. Békésy was awarded the Nobel Prize in Physiology or Medicine for his work. In 1946, the first live demonstration of tonotopic organization in auditory cortex occurred at Johns Hopkins Hospital.
More recently, advances in technology have allowed researchers to map the tonotopic organization in healthy human subjects using
electroencephalographic
Electroencephalography (EEG) is a method to record an electrogram of the spontaneous electrical activity of the brain. The biosignals detected by EEG have been shown to represent the postsynaptic potentials of pyramidal neurons in the neocort ...
(EEG) and
magnetoencephalographic (MEG) data. While most human studies agree on the existence of a tonotopic gradient map in which low frequencies are represented laterally and high frequencies are represented medially around
Heschl's gyrus
The transverse temporal gyri, also called Heschl's gyri () or Heschl's convolutions, are gyri found in the area of primary auditory cortex buried within the lateral sulcus of the human brain, occupying Brodmann areas 41 and 42. Transverse tempora ...
, a more detailed map in human auditory cortex is not yet firmly established due to methodological limitations
Sensory mechanisms
Peripheral nervous system
Cochlea
Tonotopic organization in the cochlea forms throughout pre- and post-natal development through a series of changes that occur in response to auditory stimuli. Research suggests that the pre-natal establishment of tonotopic organization is partially guided by synaptic reorganization; however, more recent studies have shown that the early changes and refinements occur at both the circuit and subcellular levels. In mammals, after the inner ear is otherwise fully developed, the tonotopic map is then reorganized in order to accommodate higher and more specific frequencies. Research has suggested that the
receptor guanylyl cyclase Npr2
Natriuretic peptide receptor B/guanylate cyclase B (atrionatriuretic peptide receptor B), also known as NPR2, is an atrial natriuretic peptide receptor. In humans it is encoded by the NPR2 gene.
A mutation of the NPR2 gene can result in dispropo ...
is vital for the precise and specific organization of this tonotopy. Further experiments have demonstrated a conserved role of
Sonic Hedgehog emanating from the notochord and floor plate in establishing tonotopic organization during early development. It is this proper tonotopic organization of the hair cells in the cochlea that allows for correct perception of frequency as the proper pitch.
Structural organization
In the
cochlea
The cochlea is the part of the inner ear involved in hearing. It is a spiral-shaped cavity in the bony labyrinth, in humans making 2.75 turns around its axis, the modiolus. A core component of the cochlea is the Organ of Corti, the sensory org ...
, sound creates a traveling
wave
In physics, mathematics, and related fields, a wave is a propagating dynamic disturbance (change from equilibrium) of one or more quantities. Waves can be periodic, in which case those quantities oscillate repeatedly about an equilibrium (res ...
that moves from base to apex, increasing in amplitude as it moves along a tonotopic axis in the
basilar membrane
The basilar membrane is a stiff structural element within the cochlea of the inner ear which separates two liquid-filled tubes that run along the coil of the cochlea, the scala media and the scala tympani. The basilar membrane moves up and down in ...
(BM).
This pressure wave travels along the BM of the cochlea until it reaches an area that corresponds to its maximum vibration frequency; this is then coded as pitch.
High frequency sounds stimulate neurons at the base of the structure and lower frequency sounds stimulate neurons at the apex.
This represents cochlear tonotopic organization. This occurs because the mechanical properties of the BM are graded along a tonotopic axis; this conveys distinct frequencies to hair cells (mechanosensory cells that amplify cochlear vibrations and send auditory information to the brain), establishing receptor potentials and, consequently frequency tuning.
For example, the BM increases in stiffness towards its base.
Mechanisms of cochlear tonotopy
Hair bundles, or the “mechanical antenna” of
hair cell
Hair cells are the sensory receptors of both the auditory system and the vestibular system in the ears of all vertebrates, and in the lateral line organ of fishes. Through mechanotransduction, hair cells detect movement in their environment. ...
s, are thought to be particularly important in cochlear tonotopy.
The morphology of hair bundles likely contributes to the BM gradient. Tonotopic position determines the structure of hair bundles in the cochlea.
The height of hair bundles increases from base to apex and the number of
stereocilia
Stereocilia (or stereovilli or villi) are non-motile apical cell modifications. They are distinct from cilia and microvilli, but are closely related to microvilli. They form single "finger-like" projections that may be branched, with normal cel ...
decreases (i.e. hair cells located at the base of the cochlea contain more stereo cilia than those located at the apex).
Furthermore, in the tip-link complex of cochlear hair cells, tonotopy is associated with gradients of intrinsic mechanical properties.
In the hair bundle, gating springs determine the open probability of mechanoelectrical ion transduction channels: at higher frequencies, these elastic springs are subject to higher stiffness and higher mechanical tension in tip-links of hair cells.
This is emphasized by the division of labor between outer and inner hair cells, in which mechanical gradients for outer hair cells (responsible for amplification of lower frequency sounds) have higher stiffness and tension.
Tonotopy also manifests in the electrophysical properties of transduction.
Sound energy is translated into neural signals through mechanoelectrical transduction. The magnitude of peak transduction current varies with tonotopic position. For example, currents are largest at high frequency positions such as the base of cochlea.
As noted above, basal cochlear hair cells have more stereocilia, thus providing more channels and larger currents.
Tonotopic position also determines the conductance of individual transduction channels. Individual channels at basal hair cells conduct more current than those at apical hair cells.
Finally, sound amplification is greater in the basal than in the apical cochlear regions because outer hair cells express the motor protein prestin, which amplifies vibrations and increases sensitivity of outer hair cells to lower sounds.
Central nervous system
Cortex
Audio frequency, otherwise known as the pitch, is currently the only characteristic of sound that is known with certainty to be topographically mapped in the central nervous system. However, other characteristics may form similar maps in the cortex such as sound intensity, tuning bandwidth, or modulation rate, but these have not been as well studied.
In the midbrain, there exist two primary auditory pathways to the auditory cortex—the lemniscal classical auditory pathway and the extralemniscal non-classical auditory pathway.
The lemniscal classical auditory pathway is tonotopically organized and consists of the central nucleus of the
inferior colliculus
The inferior colliculus (IC) (Latin for ''lower hill'') is the principal midbrain nucleus of the auditory pathway and receives input from several peripheral brainstem nuclei in the auditory pathway, as well as inputs from the auditory cortex. The ...
and the ventral
medial geniculate body projecting to primary areas in the auditory cortex. The non-primary auditory cortex receives inputs from the extralemniscal non-classical auditory pathway, which shows a diffuse frequency organization.
The tonotopic organization of the
auditory cortex
The auditory cortex is the part of the temporal lobe that processes auditory information in humans and many other vertebrates. It is a part of the auditory system, performing basic and higher functions in hearing, such as possible relations to ...
has been extensively examined and is therefore better understood compared to other areas of the auditory pathway.
Tonotopy of the auditory cortex has been observed in many animal species including birds, rodents, primates, and other mammals.
In mice, four subregions of the auditory cortex have been found to exhibit tonotopic organization. The classically divided A1 subregion has been found to in fact be two distinct tonopic regions—A1 and the dorsomedial field (DM).
Auditory cortex region A2 and the anterior audiotry field (AAF) both have tonotopic maps that runs dorsoventrally.
The other two regions of the mouse auditory cortex, the dorsoanterior field (DA) and the dorsoposterior field (DP) are non-tonotopic. While neurons in these non-tonotopic regions have a characteristic frequency, they are arranged randomly.
Studies using non-human primates have generated a hierarchical model of auditory cortical organization consisting of an elongated core consisting of three back-to-back tonotopic fields—the primary auditory field A1, the rostral field R, and the rostral temporal field RT. These regions are surrounded by belt fields (secondary) regions and higher-order parabelt fields. A1 exhibits a frequency gradient from high to low in the posterior-to-anterior direction; R exhibits a reversed gradient with characteristic frequencies from low to high in the posterior-to-anterior direction. RT has a less clearly organized gradient from high back to low frequencies.
These primary tonotopic patterns continuously extend into the surrounding belt areas.
Tonotopic organization in the human auditory cortex has been studied using a variety of non-invasive imaging techniques including magneto- and electroencephalography (
MEG/
EEG
Electroencephalography (EEG) is a method to record an electrogram of the spontaneous electrical activity of the brain. The biosignals detected by EEG have been shown to represent the postsynaptic potentials of pyramidal neurons in the neocortex ...
), positron emission tomography (
PET
A pet, or companion animal, is an animal kept primarily for a person's company or entertainment rather than as a working animal, livestock, or a laboratory animal. Popular pets are often considered to have attractive appearances, intelligence, ...
), and functional magnetic resonance imaging (
fMRI
Functional magnetic resonance imaging or functional MRI (fMRI) measures brain activity by detecting changes associated with blood flow. This technique relies on the fact that cerebral blood flow and neuronal activation are coupled. When an area o ...
). The primary tonotopic map in the human auditory cortex is along
Heschl's gyrus
The transverse temporal gyri, also called Heschl's gyri () or Heschl's convolutions, are gyri found in the area of primary auditory cortex buried within the lateral sulcus of the human brain, occupying Brodmann areas 41 and 42. Transverse tempora ...
(HG). However, various researchers have reached conflicting conclusions about the direction of frequency gradient along HG. Some experiments found that tonotopic progression ran parallel along HG while others found that the frequency gradient ran perpendicularly across HG in a diagonal direction, forming an angled V-shaped pair of gradients.
In mice
One of the well-established methods of studying tonotopic patterning in the auditory cortex during development is tone-rearing.
In mouse Primary
Auditory Cortex
The auditory cortex is the part of the temporal lobe that processes auditory information in humans and many other vertebrates. It is a part of the auditory system, performing basic and higher functions in hearing, such as possible relations to ...
(A1), different neurons respond to different ranges of frequencies with one particular frequency eliciting the largest response – this is known as the "best frequency" for a given neuron.
Exposing mouse pups to one particular frequency during the auditory critical period (postnatal day 12 to 15)
will shift the "best frequencies" of neurons in A1 towards the exposed frequency tone.
These frequency shifts in response to environmental stimuli have been shown to improve performance in perceptual behavior tasks in adult mice that were tone-reared during auditory critical period. Adult learning and critical period sensory manipulations induce comparable shifts in cortical topographies, and by definition adult learning results in increased perceptual abilities. The tonotopic development of A1 in mouse pups is therefore an important factor in understanding the neurological basis of auditory learning.
Other species also show similar tonotopic development during critical periods. Rat tonotopic develop is nearly identical to mouse, but the critical period is shifted slightly earlier,
and barn owls show an analogous auditory development in
Interaural Time Differences (ITD).
Plasticity of auditory critical period
The auditory critical period of rats, which lasts from postnatal day 11 (P11) to P13
can be extended through deprivation experiments such as white noise-rearing.
It has been shown that subsets of the tonotopic map in A1 can be held in a plastic state indefinitely by exposing the rats to white noise consisting of frequencies within a particular range determined by the experimenter.
For example, exposing a rat during auditory critical period to white noise that includes tone frequencies between 7 kHz and 10 kHz will keep the corresponding neurons in a plastic state far past the typical critical period–one study has retained this plastic state until the rats were 90 days old.
Recent studies have also found that release of the neurotransmitter norepinephrine is required for critical period plasticity in the auditory cortex, however intrinsic tonotopic patterning of the auditory cortical circuitry occurs independently from norepinephrine release.
A recent toxicity study showed that in-utero and postnatal exposure to polychlorinated biphenyl (PCB) altered overall primary auditory cortex (A1) organization, including tonotopy and A1 topography. Early PCB exposure also changed the balance of excitatory and inhibitory inputs, which altered the ability of the auditory cortex to plastically reorganize after changes in the acoustic environment, thereby altering the critical period of auditory plasticity.
Adult plasticity
Studies in mature A1 have focused on neuromodulatory influences and have found that direct and indirect vagus nerve stimulation, which triggers neuromodulator release, promotes adult auditory plasticity. Cholinergic signaling has been shown to engage 5-HT3AR cell activity across cortical areas and facilitate adult auditory plasticity. Furthermore, behavioral training using rewarding or aversive stimuli, commonly known to engage cholinergic afferents and 5-HT3AR cells, has also been shown to alter and shift adult tonotopic maps.
See also
*
Place theory (hearing) Place theory is a theory of hearing that states that our perception of sound depends on where each component frequency produces vibrations along the basilar membrane. By this theory, the pitch of a sound, such as a human voice or a musical tone, ...
*
Topographic maps
In modern mapping, a topographic map or topographic sheet is a type of map characterized by large- scale detail and quantitative representation of relief features, usually using contour lines (connecting points of equal elevation), but histori ...
References
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Neurophysiology