Magnetic fields elicited by tones and vowel formants reveal tonotopy and nonlinear summation of cortical activation

A long-latency response component (N1m) and the sustained field (SF) of the auditory evoked magnetic field elicited by two composite stimuli (a two-tone combination and a two-formant vowel) and their individually presented components (a 600-Hz and a 2100-Hz pure tone and two single-vowel formants with formant frequencies matched to the tone frequencies) were recorded using a 37-channel magnetometer. The response to the composite stimuli differed from the linear sum of the responses to the respective components in latency, equivalent dipole moment, and equivalent dipole location, suggesting an interaction among the processes elicited by the constituents of composite stimuli. Nlm and SF source locations were more medial for the response to the high tone than to the low tone and more medial for the response to the high vowel formant than to the low vowel formant. The Nlm formant sources were more lateral than the Nlm tone sources. These findings suggest that, at the level of the auditory cortex, vowels are represented in terms of both the spectral pitches determined by their most prominent harmonics and, within the latency range of the Nlm, the virtual pitch determined by the spacing of the harmonics.     

Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas

Summary The origin and laminar arrangement of the homolateral and callosal projections to the anterior (AAF), primary (AI), posterior (PAF) and secondary (AII) auditory cortical areas were studied in the cat by means of electrophysiological recording and WGA-HRP tracing techniques. The transcallosal projections to AAF, AI, PAF and AII were principally homotypic since the major source of input was their corresponding area in the contralateral cortex. Heterotypic transcallosal projections to AAF and AI were seen, originating from the contralateral AI and AAF, respectively. PAF received heterotypic commissural projections from the opposite ventroposterior auditory cortical field (VPAF). Heterotypic callosal inputs to AII were rare, originating from AAF and AI. The neurons of origin of the transcallosal connections were located mainly in layers II and III (70–92%), and less frequently in deep layers (V and VI, 8–30%). Single unit recordings provided evidence that both homotypic and heterotypic transcallosal projections connect corresponding frequency regions of the two hemispheres. The regional distribution of the anterogradely labeled terminals indicated that the homotypic and heterotypic auditory transcallosal projections are reciprocal. The present data suggest that the transcallosal auditory interconnections are segregated in 3 major parallel components (AAF-AI, PAF-VPAF and AII), maintaining a segregation between parallel functional channels already established for the thalamocortical auditory interconnections. For the intrahemispheric connections, the analysis of the retrograde tracing data revealed that AAF and AI receive projections from the homolateral cortical areas PAF, VPAF and AII, whose neurons of origin were located mainly in their deep (V and VI) cortical layers. The reciprocal interconnections between the homolateral AAF and AI did not show a preferential laminar arrangement since the neurons of origin were distributed almost evenly in both superficial (II and III) and deep (V and VI) cortical layers. On the contrary, PAF received inputs from the homolateral cortical fields AAF, AI, AII and VPAF, originating predominantly from their superficial (II and III) layers. The homolateral projections reaching AII originated mainly from the superficial layers of AAF and AI, but from the deep layers of VPAF and PAF. The laminar distribution of anterogradely labeled terminal fields, when they were dense enough for a confident identification, was systematically related to the laminar arrangement of neurons of origin of the reciprocal projection: a projection originating from deep layers was associated with a reciprocal projection terminating mainly in layer IV, whereas a projection originating from superficial layers was associated with a reciprocal projection terminating predominantly outside layer IV. This laminar distribution indicates that the homolateral auditory cortical interconnections have a feed-forward/feed-back organization, corresponding to a hierarchical arrangement of the auditory cortical areas, according to criteria previously established in the visual system of primates. The principal auditory cortical areas could be ranked into 4 distinct hierarchical levels. The tonotopically organized areas AAF and AI represent the lowest level. The second level corresponds to the non-tonotopically organized area AII. Higher, the tonotopically organized areas VPAF and PAF occupy the third and fourth hierarchical levels, respectively.Abbreviations AAF anterior auditory cortical area - AI primary auditory cortical area - AII secondary auditory cortical area - BF best frequency - C cerebral cortex - CA caudate nucleus - CL claustrum - D dorsal nucleus of the dorsal division of the MGB - ea anterior ectosylvian sulcus - ep posterior ectosylviansulcus - IC internal capsule - LGN lateral geniculate nucleus - LV pars lateralis of the ventral division of the MGB - LVe lateral ventricule - M pars magnocellularis of the medial division of the MGB - MGB medial geniculate body - MGBv ventral division of the MGB - OT optic tract - OV pars ovoidea of the ventral division of the MGB - PAF posterior auditory cortical area - PH parahippocampal cortex - PO lateral part of the posterior group of thalamic nuclei - PU putamen - RE reticular complex of thalamus - rs rhinal sulcus - SG suprageniculate nucleus of the dorsal division of the MGB - ss suprasylvian sulcus - TMB tetrametylbenzidine - VBX ventrobasal complex - VLa ventrolateral complex - VL ventro-lateral nucleus of the ventral division of the MGB - WGA-HRP wheat germ agglutinin conjugated to horse-radish peroxidase - WM white matter - VPAF ventro-posterior auditory cortical area     

Effect of sound intensity on tonotopic fMRI maps in the unanesthetized monkey

The monkey's auditory cortex includes a core region on the supratemporal plane (STP) made up of the tonotopically organized areas A1, R, and RT, together with a surrounding belt and a lateral parabelt region. The functional studies that yielded the tonotopic maps and corroborated the anatomical division into core, belt, and parabelt typically used low-amplitude pure tones that were often restricted to threshold-level intensities. Here we used functional magnetic resonance imaging in awake rhesus monkeys to determine whether, and if so how, the tonotopic maps and the pattern of activation in core, belt, and parabelt are affected by systematic changes in sound intensity. Blood oxygenation level-dependent (BOLD) responses to groups of low- and high-frequency pure tones 3–4 octaves apart were measured at multiple sound intensity levels. The results revealed tonotopic maps in the auditory core that reversed at the putative areal boundaries between A1 and R and between R and RT. Although these reversals of the tonotopic representations were present at all intensity levels, the lateral spread of activation depended on sound amplitude, with increasing recruitment of the adjacent belt areas as the intensities increased. Tonotopic organization along the STP was also evident in frequency-specific deactivation (i.e. “negative BOLD”), an effect that was intensity-specific as well. Regions of positive and negative BOLD were spatially interleaved, possibly reflecting lateral inhibition of high-frequency areas during activation of adjacent low-frequency areas, and vice versa. These results, which demonstrate the strong influence of tonal amplitude on activation levels, identify sound intensity as an important adjunct parameter for mapping the functional architecture of auditory cortex.     

Perception of complex sounds: N1 latency codes pitch and topography codes spectra.

OBJECTIVES: This work aimed to find out whether the human cortical 'tonotopy' represents the true fundamental frequency (Fo) of complex sounds, or the center frequency CF at which harmonics peak in the audio spectrum. Indeed, complex periodic sounds (such as those of the human voice, musical instruments, etc.) comprise a 'fundamental component' (Fo) and its 'harmonics' (2Fo, 3Fo, ...nFo). These often peak around a certain frequency CF. As Fo and CF are confounded in pure (sinusoidal) tones, the question of whether Fo or CF is represented through tonotopy had been hitherto unresolved. METHODS: Whole-head recordings of brain electrical activity were obtained for 16 subjects submitted to an array of 9 different series of sounds (3 Fox3 CF). Electrophysiological data were analyzed separately for each sound and each subject with brain functional imaging and dipole reconstruction. RESULTS: Equivalent dipole sources of N1 components were, significantly for all subjects, more and more frontally oriented as CF increased, independently of Fo. CONCLUSIONS: Sounds are mapped in both the right and the left primary auditory cortices according to the spectral profiles of their harmonics (CF), rather than their fundamental frequencies (Fo).     

The auditory pathway in cat corpus callosum

The cortical auditory fields of the two hemispheres are interconnected via the corpus callosum. We have investigated the topographical arrangement of auditory callosal axons in the cat. Following circumscribed biocytin injections in the primary (AI), secondary (AII), anterior (AAF) and posterior (PAF) auditory fields, labelled axons have been found in the posterior two-thirds of the corpus callosum. Callosal axons labelled by small individual cortical injections did not form a tight bundle at the callosal midsagittal plane but spread over as much as one-third of the corpus callosum. Axons originating from different auditory fields were roughly topographically ordered, reflecting to some extent the rostro-caudal position of the field of origin. Axons from AAF crossed on average more rostrally than axons from AI; the latter crossed more rostrally than axons from PAF and AIL Callosal axons originating in a discrete part of the cortex travelled first in a relatively tight bundle to the telo-diencephalic junction and then dispersed progressively. In conclusion, the cat corpus callosum does not contain a sector reserved for auditory axons, nor a strictly topographically ordered auditory pathway. This observation is of relevance to neuropsychological and neuropathological observations in man.     

Representation of the cochlea in the neocortex of guinea pigs

Summary By recording unit clusters and local evoked responses in the auditory cortex of guinea pigs the cortical representation of best frequencies was studied. In penetrations vertical to the cortical surface best frequencies were similar. Parallel to the cortical surface, however, different frequencies were found in the antero-posterior direction, whereas medio-laterally best frequencies usually remained in the same range (isofrequency stripes). Two auditory cortical fields could be distinguished, which are tonotopically organized. With increasing sound intensity the cortical response field for a given frequency and thus the frequency overlap increased. All along the isofrequency stripes in the medio-lateral direction, the stimulation of the contralateral ear produces larger responses than the same stimulus delivered to the ipsilateral ear.Partly supported by the Deutsche Forschungsgemeinschaft, SFB 33     

Does the location of a vascular loop in the cerebellopontine angle explain pulsatile and non-pulsatile tinnitus?

The purpose was to investigate patients with unexplained pulsatile and non-pulsatile tinnitus by means of MR imaging of the cerebellopontine angle (CPA) and to correlate the clinical subtype of tinnitus with the location of a blood vessel (in the internal auditory canal or at the cisternal part of the VIIIth cranial nerve). Clinical presentation of tinnitus and perceptive hearing loss were correlated. In 47 patients with unexplained tinnitus, an MR examination of the CPA was performed. Virtual endoscopy reconstructions were obtained using a 3D axial thin-section high-resolution heavily T2-weighted gradient echo constructive interference in steady state (CISS) data-set. High-resolution T2-weighted CISS images showed a significantly higher number of vascular loops in the internal auditory canal in patients with arterial pulsatile tinnitus compared to patients with non-pulsatile tinnitus (P<0.00001). Virtual endoscopy images were used to investigate vascular contacts at the cisternal part of the VIIIth cranial nerve in patients with low pitch and high pitch non-pulsatile tinnitus. A significantly different distribution of the vascular contacts (P=0.0320) was found. Furthermore, a correlation between the clinical presentation of non-pulsatile tinnitus (high pitch and low pitch) and the perceptive hearing loss was found (P=0.0235). High-resolution heavily T2-weighted CISS images and virtual endoscopy of the CPA can be used to evaluate whether a vascular contact is present in the internal auditory canal or at the cisternal part of the VIIIth cranial nerve and whether the location of the vascular contact correlates with the clinical subtype of tinnitus. Our findings suggest that there is a tonotopical structure of the cisternal part of the VIIIth cranial nerve. A correlation between the clinical presentation of tinnitus and hearing loss was found.     

Sound frequency representation in cat auditory cortex

Using the intrinsic signal optical recording technique, we reconstructed the two-dimensional pattern of stimulus-evoked neuronal activities in the auditory cortex of anesthetized and paralyzed cats. The average magnitude of intrinsic signal in response to a pure tone stimulus increased steadily as the sound pressure level increased. A detailed analysis demonstrated that the evoked signals at early frames were scaled by the sound pressure level, which in turn indicated the presence of a minimum level of sound pressure beyond which stimulus-related intrinsic signal can be generated. Intrinsic signals evoked significantly by pure tone stimuli of different frequencies were localized and arranged in an orderly manner in the middle ectosylvian gyrus, which indicates that the primary auditory field (AI) is tonotopically organized. The arrangement of optimal frequencies obtained from optical recordings of the same auditory cortex, which were conducted on different days, was highly reproducible. Furthermore, other auditory fields surrounding AI in the recorded area were allocated based on the observed tonotopicity. We also conducted unit recordings on the cats used for optical recording with the same set of acoustic stimuli. The gross feature of the arrangement of optimal frequencies determined by unit recordings agreed with the tonotopic arrangement determined by the optical recording, although the precise agreement was not obtained.     

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.     

The auditory cortex of the bat Molossus molossus: Disproportionate search call frequency representation

The extent of the auditory cortex in the bat Molossus molossus was electrophysiologically investigated. Best frequencies and minimum thresholds of neural tuning curves were analyzed to define the topography of the auditory cortex. The auditory cortex encompasses an average cortical surface area of 5 mm². Characteristic frequencies are tonotopically organized with low frequencies being represented caudally and high frequencies rostrally. However, a large interindividual variability in the tonotopic organization was found. In most animals, the caudal 50% was tonotopically organized. More anterior, a variable area was found. A distinct field with reversed topography was not consistently found. Within the demarcated auditory cortex, frequencies of 30–40 kHz, which correspond to the frequency range of search calls emitted during hunting, are overrepresented, occupying 49% of the auditory cortex surface. High minimum thresholds >50 dB SPL were found in a narrow dorsal narrow area. Neurons with multipeaked tuning curves (20%) preferentially were located in the dorsal part of the auditory cortex. In accordance with studies in other bat species, the auditory cortex of M. molossus is highly sensitive to the dominant frequencies of biosonar search calls.