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Mapping an intrinsic MR property of gray matter in auditory cortex of living humans: a possible marker for primary cortex and hemispheric differences.

Recently, magnetic resonance properties of cerebral gray matter have been spatially mapped--in vivo--over the cortical surface. In one of the first neuroscientific applications of this approach, this study explores what can be learned about auditory cortex in living humans by mapping longitudinal relaxation rate (R1), a property related to myelin content. Gray matter R1 (and thickness) showed repeatable trends, including the following: (1) Regions of high R1 were always found overlapping posteromedial Heschl's gyrus. They also sometimes occurred in planum temporale and never in other parts of the superior temporal lobe. We hypothesize that the high R1 overlapping Heschl's gyrus (which likely indicates dense gray matter myelination) reflects auditory koniocortex (i.e., primary cortex), a heavily myelinated area that shows comparable overlap with the gyrus. High R1 overlapping Heschl's gyrus was identified in every instance suggesting that R1 may ultimately provide a marker for koniocortex in individuals. Such a marker would be significant for auditory neuroimaging, which has no standard means (anatomic or physiologic) for localizing cortical areas in individual subjects. (2) Inter-hemispheric comparisons revealed greater R1 on the left on Heschl's gyrus, planum temporale, superior temporal gyrus and superior temporal sulcus. This asymmetry suggests greater gray matter myelination in left auditory cortex, which may be a substrate for the left hemisphere's specialized processing of speech, language, and rapid acoustic changes. These results indicate that in vivo R1 mapping can provide new insights into the structure of human cortical gray matter and its relation to function.

Adult↗

Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex.

How does cortex that normally processes inputs from one sensory modality respond when provided with input from a different modality? We have addressed such a question with an experimental preparation in which retinal input is routed to the auditory pathway in ferrets. Following neonatal surgical manipulations, a specific population of retinal ganglion cells is induced to innervate the auditory thalamus and provides visual input to cells in auditory cortex (Sur et al., 1988). We have now examined in detail the visual response properties of single cells in primary auditory cortex (A1) of these rewired animals and compared the responses to those in primary visual cortex (V1) of normal animals. Cells in A1 of rewired animals differed from cells in normal V1: they exhibited larger receptive field sizes and poorer visual responsivity, and responded with longer latencies to electrical stimulation of their inputs. However, striking similarities were also found. Like cells in normal V1, A1 cells in rewired animals exhibited orientation and direction selectivity and had simple and complex receptive field organizations. Furthermore, the degree of orientation and directional selectivity as well as the proportions of simple, complex, and nonoriented cells found in A1 and V1 were very similar. These results have significant implications for possible commonalities in intracortical processing circuits between sensory cortices, and for the role of inputs in specifying intracortical circuitry.

Animals↗

[An analysis of interneuronal connections in the auditory cortex of awake cats].

A statistical analysis has been made of the interaction of the auditory cortex units in alert cats with chronically implanted electrodes. Three neurones with an amplitude ratio of 4:2:1 were singled out from the multineuronal activity. The dependence between the firing of two neurones was determined by the cross interval histograms. The relationships between 78 pairs of units were studied in 26 three units microsystems. About a third of the studied pairs functioned independently. The number of pairs with one-way and two-way connections was about equal (26 and 30 respectively). The neurones which generated spikes of high and medium amplitude, had the largest number of two-way connections. One-way connections were equally represented in all the three neurones, though with regard to direction they depended on the amplitude characteristics of the spikes. In neurones with large and medium spikes, output connections predominated, while in neurones with small spikes input connections predominated considerably. The connection could be of inhibitory, excitatory or mixed type. The inhibitory type of connections was the most frequent occurrence (57 out of 86). At prolonged recording (6 to 16 min) of spike activity, most of the functional connections persisted.

Animals↗

Affects of aging on receptive fields in rat primary auditory cortex layer V neurons.

Advanced age is commonly associated with progressive cochlear pathology and central auditory deficits, collectively known as presbycusis. The present study examined central correlates of presbycusis by measuring response properties of primary auditory cortex (AI) layer V neurons in the Fischer Brown Norway rat model. Layer V neurons represent the major output of AI to other cortical and subcortical regions (primarily the inferior colliculus). In vivo single-unit extracellular recordings were obtained from 114 neurons in aged animals (29-33 mo) and compared with 105 layer V neurons in young-adult rats (4-6 mo). Three consecutive repetitions of a pure-tone receptive field map were run for each neuron. Age was associated with fewer neurons exhibiting classic V/U-shaped receptive fields and a greater percentage of neurons with more Complex receptive fields. Receptive fields from neurons in aged rats were also less reliable on successive repetitions of the same stimulus set. Aging was also associated with less firing during the stimulus in V/U-shaped receptive field neurons and more firing during the stimulus in Complex neurons, which were generally associated with inhibited firing in young controls. Finally, neurons in aged rats with Complex receptive fields were more easily driven by current pulses delivered to the soma. Collectively, these findings provide support for the notion that age is associated with diminished signal-to-noise coding by AI layer V neurons and are consistent with other research suggesting that GABAergic neurotransmission in AI may be compromised by aging.

Acoustic Stimulation↗

Representation of periodicity pitch in the primary auditory cortex of the Mongolian gerbil.

Responses of single and multi-units in the primary auditory cortex (AI) of the Mongolian gerbil to tones and amplitude modulations (AMs) were studied. Two types of AM stimuli were used: i) those which were spectrally inside the unit's frequency response range (FRR) and ii) those that were spectrally completely outside a unit's FRR. In response to AMs spectrally within a unit's FRR, a minority of units showed phase-locked responses tuned to a certain range of modulation frequencies (envelope periodicities) of the AM. Phase-locking was confined to frequencies up to 65 Hz, the range best modulation frequencies covered by this synchrony code (sync-BMFs) contained values between 5 and 30 Hz. In response to AMs completely outside a unit's FRR, 69% of the units in the low frequency area of AI (up to 3 kHz best frequency) exhibited phasic or tonic responses tuned to certain envelope periodicities with rate-BMFs ranging from 50 to about 3000 Hz, a range that might be sufficient to account for a representation of periodicity pitch. Topographic reconstruction of the recording sites of such units revealed that, in contrast to the sync-BMFs described above, the rate-BMF values were systematically distributed within AI, therefore reflecting a periodotopic organization. We suggest that the temporal quality of the percept (rhythm) might be coded via a temporal (synchrony) code whereas the non-temporal quality of the percept (pitch) is coded via a non-temporal (rate-place) code.

Animals↗

Combination-sensitive neurons in the primary auditory cortex of the mustached bat.

In the mustached bat, Pteronotus parnellii, neurons in the primary auditory cortex (AI) have been thought to respond primarily to single frequencies, as in other mammals. However, neurons in the Doppler-shifted constant-frequency (DSCF) area, a part of the mustached bat's AI that contains an overrepresentation of the prominent CF2 component of the biosonar signal, were found to show facilitative responses to combinations of different frequencies in the pulse and echo. The essential components for facilitation were the pulse FM1 and the echo CF2. The FM1-CF2 facilitation was sensitive to echo delays, indicating that DSCF neurons respond better to targets within particular ranges. On average, the longest discriminable echo delay, based on increased impulse counts due to facilitation, corresponded to a target range of 4.3 m, and the most discriminable delay corresponded to a target 3.6 m distant. Since mustached bats first show a behavioral response to a target at a distance of 3-4 m, DSCF neurons are suited to signal the presence of an insect within this behaviorally important range. DSCF neurons were broadly tuned to echo delay, with the average minimum discriminable echo delay corresponding to a target range of 1.9 m, and the delay tuning of the neurons followed (tracked) changes in pulse duration, indicating that facilitation occurs during much of the approach phase of insect pursuit when target characterization is presumably occurring. These results show that AI neurons in the mustached bat are specialized to respond to complex, behaviorally relevant stimuli during the search and approach phases of insect pursuit.

Acoustic Stimulation↗

Neuromagnetic responses to frequency-tagged sounds: a new method to follow inputs from each ear to the human auditory cortex during binaural hearing.

Binaural cortical responses are mixtures of inputs from both ears. We introduce here a novel method that allows, for the first time, to selectively follow these inputs in humans up to the cortex during binaural hearing. We recorded neuromagnetic cortical responses to amplitude-modulated continuous tones, with different modulation frequencies at each ear. During binaural hearing, the left- and right-ear inputs competed strongly in both auditory cortices: the right-hemisphere responses were symmetrically suppressed, compared with monaural stimulation, for sounds of both ears, whereas the left-hemisphere responses were suppressed significantly more for ipsilateral than contralateral sounds, thereby intensifying the right-ear dominance of the left auditory cortex. This type of hemisphere- and ear-selective information on cortical binaural interaction could have important applications in human auditory neuroscience.

Acoustic Stimulation↗

Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. II. Repetition rate coding.

1. Responses of neurons in primary auditory cortex (AI) of the barbiturate-anesthetized adult cat were studied using cochlear stimulation with electrical and acoustic stimuli. Neuronal responses to acoustic stimulation with brief biphasic clicks of the ear ipsilateral to the studied cortical hemisphere were compared with those evoked by electrical stimulation of the contralateral cochlea with brief biphasic electrical pulses delivered via a feline cochlear prosthesis. The contralateral ear was deafened immediately before implantation of the cochlear prosthesis. The feline cochlear prosthesis consisted of four bipolar electrode pairs and was placed in the scala tympani. Two bipolar electrode conditions were used for stimulation: one near radial pair with electrode spacing of 0.25-0.5 mm, and one longitudinal pair with electrode spacing of approximately 6 mm. 2. The firing rates obtained from single- and multiple-neuron recordings were measured as a function of stimulus repetition rate of electrical and acoustic pulses. From period histograms over a recording interval of 1,000 ms, the driven firing rate to repetition rates from 2 to 38 Hz was obtained and repetition rate transfer functions (RRTFs) were constructed. The RRTFs were characterized as low-pass or band-pass filters and several descriptors were obtained, such as the repetition rate producing the highest driven activity, high and low cutoff frequencies 6 dB below maximum firing rate, and maximum firing rate. 3. For a given neuron, the main characteristics of cortical RRTFs obtained with electrical and acoustic cochlear stimulation were quite similar. However, some small but statistically significant differences in the best repetition rate, cutoff frequencies, and maximum firing rate could be observed between the different stimulation modes. The proportion of band-pass RRTFs was larger for electrical stimulation (57%) than for acoustic stimulation (41%). The high cutoff frequencies for electrical stimulation were slightly but consistently higher than for acoustic RRTFs of the same neuron and the maximum firing rate for electrical stimulation was significantly higher than that evoked by ipsilateral acoustic stimulation. 4. The entrainment of cortical neurons to electrical and acoustic pulses was determined and entrainment profiles were constructed. For a given neuron, electrical entrainment profiles showed higher cutoff frequencies than with acoustic stimulation when judged with a fixed entrainment criterion of 0.25 spikes per event. The maximum entrainment seen for electrical stimulation was approximately 20% higher than seen for the same neuron with acoustic stimulation. 5. Correlation analysis of repetition coding and latency parameters revealed several relationships between these response aspects. Most prominent among them was a significant correlation between measures of the response latency and estimates of the ability to follow temporal repetitions for acoustic as well as electrical conditions. 6. Parametric and comparative evaluations of cortical responses to acoustic and electrical cochlear stimulation support the conclusion that the temporal resolution seen in cortical neurons is largely a consequence of central processing mechanisms based on cell and circuit properties and to a lesser degree a consequence of particular spatial and temporal peripheral excitation patterns. The slightly higher temporal resolution found for the electrical stimulation modes suggests that the temporally highly coherent electrical stimulation appears to engage, in a more effective manner, the excitatory/inhibitory mechanisms contributing to the response in AI than acoustic click stimulation with less temporal coherence. (ABSTRACT TRUNCATED)

Acoustic Stimulation↗

Inner hair cell loss and steady-state potentials from the inferior colliculus and auditory cortex of the chinchilla.

Steady-state evoked potentials were measured from unanesthetized chinchillas both before and after carboplatin-induced selective inner hair cell loss. Recordings were made from both the inferior colliculus (IC) and the auditory cortex (AC). The steady-state potential was measured in the form of the envelope following response (EFR), obtained by presenting a two-tone stimulus (f1 = 2000 Hz; f2 = 2020, 2040, 2080, 2160, or 2320 Hz), and measuring the magnitude of the Fourier coefficient at the f2-f1 difference frequency. From the IC, precarboplatin, EFR amplitude vs difference tone frequency showed a bandpass pattern, with maximum amplitude at either 160 or 80 Hz, depending upon stimulus level. Postcarboplatin, the preferred difference frequency was 80 Hz for all stimulus levels. From the AC, EFR amplitude versus difference tone frequency also showed a bandpass pattern, with the maximum amplitude at 80 Hz both pre- and postcarboplatin. EFR amplitude from the IC was decreased for some conditions postcarboplatin, while the amplitude from the AC showed no significant change.

Animals↗

Sensory and cognitive mechanisms for preattentive change detection in auditory cortex.

In order to react adequately to potentially relevant information outside the focus of attention, our brain preattentively scans the acoustic environment for irregularities. Two different mechanisms are currently discussed: (i) a sensory one based on differential states of refractoriness of neurons sensitive to the features of a regular event and of neurons sensitive to features of an irregular event; (ii) a cognitive one based on a comparison of short-lived memory representations encoding current stimulation and the invariance inherent in recent recurrent stimulation. Here, we identified regions that mediate either of the two mechanisms by combining functional magnetic resonance imaging with an experimental protocol controlling for refractoriness. The sensory mechanism was associated with activity in the primary auditory cortex, whereas the cognitive one revealed activity in nonprimary auditory areas in the anterior part of Heschl's Gyrus. Moreover, it turned out that in the traditional oddball paradigm both mechanisms contribute to irregularity detection.

Acoustic Stimulation↗

Enhanced activation of the auditory cortex in patients with inner-ear hearing impairment: a magnetoencephalographic study.

OBJECTIVE: Injury of peripheral auditory organ often induces abnormality of loudness sensation such as loudness recruitment. However, objective evaluation of this phenomenon has rarely been performed. To elucidate this abnormal loudness sensation, cortical mechanisms were investigated by recording auditory evoked magnetic fields (AEFs). METHODS: We recorded AEFs in 8 patients suffering from inner-ear hearing impairment with loudness recruitment and in 14 healthy hearing controls using a 122-channel whole-head neuromagnetometer. Tone bursts of 1 kHz were presented monaurally at 4 different intensities (40, 50, 60, 70 dB HL) with a constant interstimulus interval of 1 s. RESULTS: In both groups, the 100 ms response (N100m) increased in amplitude and decreased in latency as a function of stimulus intensity in both hemispheres. Concerning the source strength, increment of dipole moment of N100m was more rapid according to the stimulus intensity in patients compared with that in healthy subjects. Source strength of N100m was enhanced at high stimulus intensity in patients, and its ratio to healthy subjects was 1.08 at 50 dB, 1.69 at 60 dB and 2.04 at 70 dB. CONCLUSIONS: In patients with inner-ear hearing impairment, enhanced activation of the auditory cortex was observed, and may help explain loudness recruitment.

Acoustic Stimulation↗

Temporal plasticity in the primary auditory cortex induced by operant perceptual learning.

Processing of rapidly successive acoustic stimuli can be markedly improved by sensory training. To investigate the cortical mechanisms underlying such temporal plasticity, we trained rats in a 'sound maze' in which navigation using only auditory cues led to a target location paired with food reward. In this task, the repetition rate of noise pulses increased as the distance between the rat and target location decreased. After training in the sound maze, neurons in the primary auditory cortex (A1) showed greater responses to high-rate noise pulses and stronger phase-locking of responses to the stimuli; they also showed shorter post-stimulation suppression and stronger rebound activation. These improved temporal dynamics transferred to trains of pure-tone pips. Control animals that received identical sound stimulation but were given free access to food showed the same results as naive rats. We conclude that this auditory perceptual learning results in improvements in temporal processing, which may be mediated by enhanced cortical response dynamics.

Acoustic Stimulation↗

Image-to-sound conversion: experience-induced plasticity in auditory cortex of blindfolded adults.

The ability to adapt to environmental changes is based on the impressive capacity of the central nervous system for plasticity changes. A better understanding of the requirements of neuroplasticity will help to apprehend and predict the success of sensory prostheses. To investigate neuroplastic changes associated with (1) blindfolding and (2) the use of a mobile visual-auditory substitution system, five normally sighted adults underwent weekly measurements of neuromagnetic activity using a 122-channel whole head neuromagnetometer. The substitution device converted visual images into sound patterns. During measurements subjects listened to "geometric sounds" converted from images of geometric shapes, "natural sounds" representing photographs of everyday objects, as well as to original "environmental sounds". To assess the role of visual deprivation, three individuals were blindfolded throughout a 3-week testing period. To assess the effect of extended exposure to "visual sounds", three subjects-two blindfolded, one sighted-had free use of the substitution device. Neuromagnetic responses were restricted to the auditory cortex across all measurements. Activity at 100 ms after presentation of "natural sounds", but not other auditory stimuli, showed a significant enhancement over time only in blindfolded subjects using the substitution system, indicating that the combination of visual deprivation and practice facilitated intra-modal plasticity. The fact that changes occurred only in response to "natural sounds" probably reflects the increased behavioural relevance of this category evident only for blindfolded subjects using the substitution device.

Acoustic Stimulation↗

Frequency organization of delay-sensitive neurons in the auditory cortex of the FM bat, Myotis lucifugus.

1. The little brown bat, Myotis lucifugus, employs biosonar pulses containing broadband frequency-modulated (FM) sounds of only one harmonic during the initial phases of echolocation. Neurons throughout the auditory cortex exhibit delay-dependent facilitation to artificial pulses and echoes at particular echo delays. Extracellular unit recordings of these delay-sensitive neurons determined the essential frequency components in the sound pair and their relative timing for evoking maximum facilitation. 2. The entire 60-kHz sweep of both the simulated pulse and echo were divided into four equal spectral quarters (Ist, IInd, IIIrd, and IVth), each linearly sweeping 15 kHz downward in 1 ms, to determine the spectral parts essential for maximal facilitation. Maximal facilitation was evoked equally by pulse-echo pairs in which the sound components consisted of either the entire 60-kHz FM sweeps or only the essential quarters. Most neurons required the IVth quarter of the pulse and the echo for delay sensitivity. This is consistent with the hypothesis that the essential quarters swept excitatory frequencies just above inhibitory frequencies. 3. The spectral and temporal contributions to delay sensitivity were examined independently. The spectral content for each spectral quarter of echo was varied in echo delay, and the sound-pair responses were compared. Maximal facilitation in individual delay-sensitive neurons required both a specific part of the echo spectrum and a specific echo delay. 4. The FM sweeps of the essential pulse and echo quarters were further narrowed to their minimum bandwidth, and the essential pulse frequencies (EPFs) and essential echo frequencies (EEFs) were determined. Both the EPFs and EEFs averaged approximately 8 kHz in FM bandwidth and represented different spectral parts of the echolocation pulse emitted by this FM bat. All neurons showed delay sensitivity to search stimuli in which pulse-echo stimuli consisted of 15-kHz FM pairs. 5. Delay sensitivity in virtually all neurons required pulse and echo components whose essential frequencies differed. However, some spectral overlap was found between the pulse and echo in 39% of these neurons. The majority of neurons (81%) required a pulse and echo in which their mean frequencies differed by < or = 16 kHz. This includes neurons with pulse and echo overlapping spectrally and those with sound components showing no overlap but separated by a relatively small frequency range. 6. The facilitative frequency-tuning curves of individual neurons were measured with their essential pulse and echo frequencies.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Topography of intensity tuning in cat primary auditory cortex: single-neuron versus multiple-neuron recordings.

1. We studied the spatial distributions of amplitude tuning (monotonicity of rate-level functions) and response threshold of single neurons along the dorsoventral extent of cat primary auditory cortex (AI). To pool data across animals, we used the multiple-unit map of monotonicity as a frame of reference. Amplitude selectivity of multiple units is known to vary systematically along isofrequency contours, which run roughly in the dorsoventral direction. Clusters sharply tuned for intensity (i.e., "nonmonotonic" clusters) are located near the center of the contour. A second nonmonotonic region can be found several millimeters dorsal to the center. We used the locations of these two nonmonotonic regions as reference points to normalize data across animals. Additionally, to compare this study to sharpness of frequency tuning results, we also used multiple-unit bandwidth (BW) maps as references to pool data. 2. The multiple-unit amplitude-related topographies recorded in previous studies were confirmed. Pooled multiple-unit maps closely approximated the previously reported individual case maps when the multiple-unit monotonicity or the map of bandwidth (in octaves) of pure tones to which a cell responds 40 dB above minimum threshold were used as the pooling reference. When the map of bandwidth (in octaves) of pure tones to which a cell responds 10 dB above minimum threshold map was used as part of the measure, the pooled spatial pattern of multiple-unit activity was degraded. 3. Single neurons exhibited nonmonotonic rate-level functions more frequently than multiple units. Although common in single-neuron recordings (28%), strongly nonmonotonic recordings (firing rates reduced by > 50% at high intensities) were uncommon (8%) in multiple-unit recordings. Intermediately nonmonotonic neurons (firing rates reduced between 20% and 50% at high intensities) occurred with nearly equal probability in single-neuron (28%) and multiple-unit (26%) recordings. The remaining recordings for multiple units (66%) and single units (44%) were monotonic (firing rates within 20% of the maximum at the highest tested intensity). 4. In ventral AI (AIv), the topography of monotonicity for single units was qualitatively similar to multiple units, although single units were on average more intensity selective. In dorsal AI (AId) we consistently found a spatial gradient for sharpness of intensity tuning for multiple units; however, for pooled single units in Aid there was no clear topographic gradient. 5. Response (intensity) thresholds of single neurons were not uniformly distributed across the dorsoventral extent of AI.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials↗

Long-latency neurons in auditory cortex involved in temporal integration: theoretical analysis of experimental data.

A previous experimental study (He et al., 1997) found 132 duration-selective neurons with long latencies of greater than 30 ms in the dorsal zone of cat auditory cortex. The mechanism by which such long-latency neurons integrate information during their latent period is investigated by analysis of the temporal relationship between the stimulus and neuronal response. In the present study, we developed a one-layer perceptron to examine the above temporal relationship of the experimental results. The acoustic stimulus was represented as a contiguous series of sequential short time epochs. The perceptron was trained by using the spike data as the desired outputs and the acoustic stimuli (in digital format) as the inputs. The adaptive weights between the outputs and the inputs after training indicated the temporal relationship between neuronal responses and the stimuli. The contribution of each time epoch of the stimulus could be either positive or negative: the positive contribution corresponds to excitatory input and the negative contribution to inhibitory input. Long-duration-selective neurons were found to receive mainly excitatory input along the entire effective stimulus duration. However, duration-tuned neurons received excitatory input for only the time period from the stimulus onset to their best durations, and inhibitory thereafter. The temporal integration pattern of short-duration-selective neurons was similar to duration-tuned neurons. However, short-duration-selective neurons received excitatory input only at the beginning of the stimulus. Each of the duration-threshold neurons integrated auditory information only for a restricted time period of the stimulus, suggesting that they have a time window over the stimulus time domain. Non-duration-threshold neurons have time windows extending from the stimulus onset onward. The assembly of duration-threshold neurons and non-duration-threshold neurons may collectively represent the time axis of the stimulus.

Acoustic Stimulation↗

Congenital auditory deprivation reduces synaptic activity within the auditory cortex in a layer-specific manner.

The present study investigates the functional deficits of naive auditory cortices in adult congenitally deaf cats. For this purpose, their auditory system was stimulated electrically using cochlear implants. Synaptic currents in cortical layers were revealed using current source density analyses. They were compared with synaptic currents found in electrically stimulated hearing cats. The naive auditory cortex showed significant deficits in synaptic activity in infragranular cortical layers. Furthermore, there was also a deficit of synaptic activities at longer latencies (>30 ms). The 'cortical column' was not activated in the well-defined sequence found in normal hearing cats. These results demonstrate functional deficits as a consequence of congenital auditory deprivation. Similar deficits are likely in congenitally deaf children.

Animals↗