Tonotopic Organization Of Auditory Cortex Research Articles

Tonotopic organization of auditory cortex in awake marmosets revealed by multi-modal wide-field optical imaging

Tonotopic organization of the auditory cortex has been extensively studied in many mammalian species using various methodologies and physiological preparations. Tonotopy mapping in primates, however, is more limited due to constraints such as cortical folding, use of anesthetized subjects, and mapping methodology. Here we applied a combination of through-skull and through-window intrinsic optical signal imaging, wide-field calcium imaging, and neural probe recording techniques in awake marmosets (Callithrix jacchus), a New World monkey with most of its auditory cortex located on a flat brain surface. Coarse tonotopic gradients, including a recently described rostral-temporal (RT) to parabelt gradient, were revealed by the through-skull imaging of intrinsic optical signals and were subsequently validated by single-unit recording. Furthermore, these tonotopic gradients were observed with more detail through chronically implanted cranial windows with additional verifications on the experimental design. Moreover, the tonotopy mapped by the intrinsic-signal imaging methods was verified by wide-field calcium imaging in an AAV-GCaMP labeled subject. After these validations and with further effort to expand the field of view more rostrally in both windowed and through-skull subjects, an additional putative tonotopic gradient was observed more rostrally to the area RT, which has not been previously described by the standard model of tonotopic organization of the primate auditory cortex. Together, these results provide the most comprehensive data of tonotopy mapping in an awake primate species with unprecedented coverage and details in the rostral proportion and support a caudal-rostrally arranged mesoscale organization of at least three repeats of functional gradients in the primate auditory cortex, similar to the ventral stream of primate visual cortex.

Tinnitus: animal models and findings in humans.

Chronic tinnitus (ringing of the ears) is a medically untreatable condition that reduces quality of life for millions of individuals worldwide. Most cases are associated with hearing loss that may be detected by the audiogram or by more sensitive measures. Converging evidence from animal models and studies of human tinnitus sufferers indicates that, while cochlear damage is a trigger, most cases of tinnitus are not generated by irritative processes persisting in the cochlea but by changes that take place in central auditory pathways when auditory neurons lose their input from the ear. Forms of neural plasticity underlie these neural changes, which include increased spontaneous activity and neural gain in deafferented central auditory structures, increased synchronous activity in these structures, alterations in the tonotopic organization of auditory cortex, and changes in network behavior in nonauditory brain regions detected by functional imaging of individuals with tinnitus and corroborated by animal investigations. Research on the molecular mechanisms that underlie neural changes in tinnitus is in its infancy and represents a frontier for investigation.

Auditory Neuroscience: Temporal Anticipation Enhances Cortical Processing

A recent study shows that expectation about the timing of behaviorally-relevant sounds enhances the responses of neurons in the primary auditory cortex and improves the accuracy and speed with which animals respond to those sounds.

Evidence of a Tonotopic Organization of the Auditory Cortex in Cochlear Implant Users

Deprivation from normal sensory input has been shown to alter tonotopic organization of the human auditory cortex. In this context, cochlear implant subjects provide an interesting model in that profound deafness is made partially reversible by the cochlear implant. In restoring afferent activity, cochlear implantation may also reverse some of the central changes related to deafness. The purpose of the present study was to address whether the auditory cortex of cochlear implant subjects is tonotopically organized. The subjects were thirteen adults with at least 3 months of cochlear implant experience. Auditory event-related potentials were recorded in response to electrical stimulation delivered at different intracochlear electrodes. Topographic analysis of the auditory N1 component (approximately 85 ms latency) showed that the locations on the scalp and the relative amplitudes of the positive/negative extrema differ according to the stimulated electrode, suggesting that distinct sets of neural sources are activated. Dipole modeling confirmed electrode-dependent orientations of these sources in temporal areas, which can be explained by nearby, but distinct sites of activation in the auditory cortex. Although the cortical organization in cochlear implant users is similar to the tonotopy found in normal-hearing subjects, some differences exist. Nevertheless, a correlation was found between the N1 peak amplitude indexing cortical tonotopy and the values given by the subjects for a pitch scaling task. Hence, the pattern of N1 variation likely reflects how frequencies are coded in the brain.

Basal Forebrain Cholinergic Input Is Not Essential for Lesion-Induced Plasticity in Mature Auditory Cortex

The putative role of the basal forebrain cholinergic system in mediating lesion-induced plasticity in topographic cortical representations was investigated. Cholinergic immunolesions were combined with unilateral restricted cochlear lesions in adult cats, demonstrating the consequence of cholinergic depletion on lesion-induced plasticity in primary auditory cortex (AI). Immunolesions almost eliminated the cholinergic input to AI, while cochlear lesions produced broad high-frequency hearing losses. The results demonstrate that the near elimination of cholinergic input does not disrupt reorganization of the tonotopic representation of the lesioned (contralateral) cochlea in AI and does not affect the normal representation of the unlesioned (ipsilateral) cochlea. It is concluded that cholinergic basal forebrain input to AI is not essential for the occurrence of lesion-induced plasticity in AI.

Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat.

Spontaneous and tone-evoked changes in light reflectance were recorded from primary auditory cortex (A1) of anesthetized cats (barbiturate induction, ketamine maintenance). Spontaneous 0.1-Hz oscillations of reflectance of 540- and 690-nm light were recorded in quiet. Stimulation with tone pips evoked localized reflectance decreases at 540 nm in 3/10 cats. The distribution of patches "activated" by tones of different frequencies reflected the known tonotopic organization of auditory cortex. Stimulus-evoked reflectance changes at 690 nm were observed in 9/10 cats but lacked stimulus-dependent topography. In two experiments, stimulus-evoked optical signals at 540 nm were compared with multiunit responses to the same stimuli recorded at multiple sites. A significant correlation (P < 0.05) between magnitude of reflectance decrease and multiunit response strength was evident in only one of five stimulus conditions in each experiment. There was no significant correlation when data were pooled across all stimulus conditions in either experiment. In one experiment, the spatial distribution of activated patches, evident in records of spontaneous activity at 540 nm, was similar to that of patches activated by tonal stimuli. These results suggest that local cerebral blood volume changes reflect the gross tonotopic organization of A1 but are not restricted to the sites of spiking neurons.

Frequency-dependent responses exhibited by multiple regions in human auditory cortex

Recordings in experimental animals have detailed the tonotopic organization of auditory cortex, including the presence of multiple tonotopic maps. In contrast, relatively little is known about tonotopy within human auditory cortex, for which even the number and location of tonotopic maps remains unclear. The present study begins to develop a more complete picture of cortical tonotopic organization in humans using functional magnetic resonance imaging, a technique that enables the non-invasive localization of neural activity in the brain. Subjects were imaged while listening to lower- (below 660 Hz) and higher- (above 2490 Hz) frequency stimuli presented alternately and at moderate intensity. Multiple regions on the superior temporal lobe exhibited responses that depended upon stimulus spectral content. Eight of these ‘frequency-dependent response regions’ (FDRRs) were identified repeatedly across subjects. Four of the FDRRs exhibited a greater response to higher frequencies, and four exhibited a greater response to lower frequencies. Based upon the location of the eight FDRRs, a correspondence is proposed between FDRRs and anatomically defined cortical areas on the human superior temporal lobe. Our findings suggest that a larger number of tonotopically organized areas exist (i.e., four or more) in the human auditory cortex than was previously recognized.

Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys

Microelectrode recordings were used to investigate the tonotopic organization of auditory cortex of macaque monkeys and guide the placement of injections of wheat germ agglutinin-horse radish peroxidase (WGA-HRP) and fluorescent dyes. Anatomical and physiological results were later related to histological distinctions in the same brains after sections were processed for cytoarchitecture, myeloarchitecture, acetylcholinesterase (AchE), or cytochrome oxidase (CO). The experiments produced several major findings. (1) Neurons throughout a broad expanse of cortex were highly responsive to pure tones, and best frequencies could be determined for neurons in arrays of recording sites. (2) The microelectrode recordings revealed two systematic representations of tone frequencies, the primary area (AI) and a primary-like rostral field (R) as previously described. The representation of high to low frequency tones in A1 was largely caudorostral along the plane of the sulcus. A reversal of the order of representation of frequencies occurred in R. (3) AI and R together were coextensive with a koniocellular, densely myelinated zone that expressed high levels of AchE and CO. These architectonic features were somewhat less pronounced in R than AI, but a clear border between the two areas was not apparent. (4) Cortex bordering AI and R was less responsive to tones, but when best frequencies for neurons could be determined, they matched those for adjoining parts of AI and R. (5) Architectonically distinct regions were apparent within some of the cortex bordering AI and R. (6) The major ipsilateral cortical connections of AI were with R and cortex immediately lateral and medial to AI. (7) Callosal connections of AI were predominantly with matched locations in the opposite AI, but they also included adjoining fields. (8) Neurons in the ventral (MGV), medial (MGM), and dorsal (MGD) nuclei of the medial geniculate complex projected to AI and cortex lateral to AI. (9) Injections in cortex responsive to high frequency tones labeled more dorsal parts of MGV than injections in cortex responsive to low frequency tones.

Tonotopic organization of the auditory cortex: pitch versus frequency representation.

According to the place principles of the classical hearing theory, the physical entity frequency is encoded in the auditory periphery as place information (tonotopic representation), which is decoded in more central parts of the auditory system to form the subjective entity pitch. However, this relation is true only for pure-tone signals (spectral pitch); it can be quite different in the case of complex auditory stimuli (virtual pitch), thus requiring a multistage process for pitch formation. Neuromagnetic measurements showed that the tonotopic organization of the primary auditory cortex reflects the pitch rather than the frequency of the stimulus; that is, the pitch formation process must take place in subcortical regions.

Tonotopic organization in auditory cortex of the cat.

Microelectrode mapping techniques were employed in the cat's auditory cortex to relate the best frequencies of a large population of neurons with their spatial loci. Based upon the best-frequency distribution, the auditory region was divided into four complete and orderly tonotopic representations and a surrounding belt of cortex in which the tonotopic organization was more complex. The four auditory fields occupy a crescent-shaped band of tissue which comprises portions of both the exposed gyral surfaces and sulcal banks of the ectosylvian cortex. The anterior auditory field (A) is situated most rostrally upon the anterior ectosylvian gyrus. It extends upon the ventral bank of the suprasylvian sulcus and upon the banks of the anterior ectosylvian sulcus. Adjoining field A caudally is the primary auditory field (AI), which extends across the middle ectosylvian gyrus and portions of both banks of the posterior ectosylvian sulcus. The representations of the highest best frequencies in fields A and AI are contiguous. Caudal and ventral to AI are located the posterior (P) and ventroposterior (VP) auditory fields. They lie mainly upon the caudal bank of the posterior ectosylvian sulcus but also extend upon the rostral bank and upon the posterior ectosylvian gyrus. The low best-frequency representations of fields AI and P are contiguous, whereas the low best-frequency representation of field VP lies near the ventral end of the posterior ectosylvian sulcus. Fields P and VP are joined along their middle and high best-frequency representations. Within each auditory field isofrequency lines defined by the spatial loci of neurons with similar best frequencies are oriented orthogonal to the low-to-high best-frequency gradients.

Tonotopic Organization of the Cat Auditory Cortex for Some Complex Stimuli

There is psychophysical evidence that both spectrum and periodicity of acoustic signals may be cues for pitch judgments. At the level of the auditory nerve, these stimulus characteristics seem to be coded in terms of place and time pattern. Very little is known of their representation higher levels of the nervous system. Tonotopic organization of the auditory cortex has been demonstrated in anesthetized cats by the evoked strychnine potential technique. In these demonstrations only tonal stimuli were used. We use similar physiological preparations but employ acoustic stimuli that permit independent manipulation of spectrum and periodicity. The results show that the previously reported tonotopic organization is based only upon spectral characteristics of the stimulus.

An electrophysiological determination of tonotopic organization in auditory cortex of cat.

An electrophysiological determination of tonotopic organization in auditory cortex of cat.