'What', 'where' and 'how' in auditory cortex.
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The topographical response of a portion of an isofrequency contour in primary cat auditory cortex (AI) to a series of monaural and binaural stimuli was studied. Responses of single neurons to monaural and a matrix of binaural characteristic frequency tones, varying in average binaural level (ABL) and interaural level differences (ILD), were recorded. The topography of responses to monaural and binaural stimuli was appreciably different. Patches of cells that responded monotonically to increments in ABL alternated with patches that responded nonmonotonically to ABL. The patches were between 0.4 and 1 mm in length along an isofrequency contour. Differences were found among monotonic patches and among nonmonotonic patches. Topographically, activated and silent populations of neurons varied with both changes in ILD and changes in ABL, suggesting that the area of responsive units may underlie the coding of sound level and sound location.
The leftward hemispheric dominance in language processing may be associated with fundamental functional asymmetry in the primary auditory cortex (PAC). Based on repeated functional MRI (fMRI) measurements, we investigated the presence of functional asymmetry in the human PAC using binaural presentation of linguistic sounds (two-syllable nouns) and simple tonal stimulation. Eight right-handed volunteers underwent nine fMRI sessions, approximately eight weeks apart, spanning the duration of more than a year. The PAC from each hemisphere was manually segmented and the volume of activation, detected within the segmented region-of-interest, was measured across the subjects and sessions to generate functional laterality indices. Although variations existed in activation volume between sessions and subjects, we found predominant and consistent leftward functional asymmetry in PAC during both linguistic and non-linguistic sound stimulations.
In experiments on cats anaesthetized with nembutal it was shown by intracellular recordings that neurons located in the primary auditory cortex respond to characteristic frequency tones or to electrical stimulation of spiral ganglion fibres innervating the centre of the neuronal receptive field by a short latency spike response followed by long-lasting (20-250 ms) poststimulus inhibition. The cause of this inhibition is an IPSP originating in the studied neuron after the spike. On the basis of close connection between poststimulus inhibition and preceding spike activity the conclusion is made that the inhibition is created by a recurrent mechanism. When tones of noncharacteristic frequencies were used or peripheral parts of the receptive field were stimulated, responses in form of EPSP-IPSP developed. They were followed by depression of neuronal background activity and its responses to test stimuli. It was shown that these effects are produced by the mechanism of lateral inhibition. The characteristics of these two kinds of inhibition are presented.
In the tangential plane (parallel to the pial surface) dendrites in the primary auditory cortex (A1) of cat were found to exhibit preferentially oriented growth. This was shown by means of a computer microscope study of Golgi-Cox stained neurons as seen in 100 micrometers and 300 micrometers thick tangential sections. Two techniques were used to represent the 3-dimensional structure of dendrites: the "dendritic stick" and the "dendritic trumpet". The former dismembers a dendrite into its individual segments; the latter considers a dendrite as an entity and represents it by its centroid, its moments and the spatial dispersionof its branches. Both statistical and Fourier analyses of the data show that within the tangential plane there is a significant and consistent orientation of the dendritic sticks in a dorso-ventral direction which seems correlated with the cortical isofrequency contours observed in electrophysiological maps of the A1 region. The dendritic trumpet analyses also show a distinctly non-random vertical distribution of pyramidal cell basal dendrites but not of stellate cell dendrites.
The effects of conditioning on the discharges of single neurons in primary auditory cortex (AI) were determined during acquisition of the pupillary conditioned response in chronically prepared cats. Acoustic stimuli (1-s white noise or tone) were presented with electrodermal stimulation unpaired during a sensitization control phase followed by pairing during a subsequent conditioning phase. Stimulus constancy at the periphery was ensured by the use of neuromuscular blockade. Discharge plasticity developed rapidly for both evoked and background activity, the former attaining criterion faster than the latter. The pupillary dilation conditioned response was acquired at the same rate as were changes in evoked activity (i.e., 10-15 trials) and faster than background activity (i.e., 20-25 trials). Increases in background activity were correlated with increasing level of tonic arousal, as indexed by pretrial size of the pupil.
Speech comprehension depends on the integrity of both the spectral content and temporal envelope of the speech signal. Although neural processing underlying spectral analysis has been intensively studied, less is known about the processing of temporal information. Most of speech information conveyed by the temporal envelope is confined to frequencies below 16 Hz, frequencies that roughly match spontaneous and evoked modulation rates of primary auditory cortex neurons. To test the importance of cortical modulation rates for speech processing, we manipulated the frequency of the temporal envelope of speech sentences and tested the effect on both speech comprehension and cortical activity. Magnetoencephalographic signals from the auditory cortices of human subjects were recorded while they were performing a speech comprehension task. The test sentences used in this task were compressed in time. Speech comprehension was degraded when sentence stimuli were presented in more rapid (more compressed) forms. We found that the average comprehension level, at each compression, correlated with (i) the similarity between the frequencies of the temporal envelopes of the stimulus and the subject's cortical activity ("stimulus-cortex frequency-matching") and (ii) the phase-locking (PL) between the two temporal envelopes ("stimulus-cortex PL"). Of these two correlates, PL was significantly more indicative for single-trial success. Our results suggest that the match between the speech rate and the a priori modulation capacities of the auditory cortex is a prerequisite for comprehension. However, this is not sufficient: stimulus-cortex PL should be achieved during actual sentence presentation.
The usefulness of dipole models in interpreting neuromagnetic field patterns was studied. By statistical means it turned out to be difficult to differentiate between a point-like source and an extended source at the auditory cortex. A single dipole is an appropriate source model for localized cortical activity extending up to a few square centimeters. Additional information about the source configuration can be obtained by focusing the analysis on areas where the differences between patterns produced by different sources should theoretically be the largest.
The corpus callosum was sectioned in groups of rats 3, 12, and 24 months of age, and the auditory cortex was examined three months later to determine whether there were age-related differences in the morphological response to the partial deafferentation. Material from the three groups of long-term callosally-lesioned rats were compared with three groups of age-matched control animals. Analysis focused on those cortical layers known to receive the heaviest callosal projection (layers II and III) and those neurons known to be postsynaptic to callosal afferents (layer V pyramidal neurons). There were no age-related changes in cortical thickness or in the relative thickness of the cortical layers in the control groups. However, the apical dendrites of layer V pyramidal neurons did lose dendritic spines and became thinner with age. In all three lesion groups, the cortex became thinner without altering the relative thickness of cortical layers; there was a decrease in the relative density of apical dendrite spines in layer III, but an increase in the density of these spines in layer IV. Both effects varied with age. Spine decreases in layer III were greatest in older animals and spine increases in layer IV were greatest in younger animals. The mean diameters of apical dendrites decreased in the youngest group of lesioned animals but increased in the oldest group. The results indicate that the effects of callosal deafferentation are age dependent.
Small iontophoretic injections, of the leucoagglutinin extracted from Phaseolus vulgaris (PHA-L), were made at a depth of 600 microns, into the ferret primary auditory cortex (AI). The lectin anterogradely labelled the axons of pyramidal cells located in the upper layers. The axons had collaterals which terminated in 5-8 columns within AI. The columns were 0.25-0.8 mm in diameter and, based on their position, appeared to be in areas of cortex where the cells would have higher and lower as well as equivalent characteristic frequencies to those in the injection site.
With optical recording of intrinsic signals (ORIS) and tone stimulation, we analysed frequency- and intensity-dependent spatio-temporal activity in primary auditory cortex AE of awake Mongolian gerbils. We found a two-dimensional and assymetric propagation of ORIS activity (1) from ventral to dorsal along isofrequency contours at all frequencies and (2) from the low-frequency end across the complete tonotopic gradient at low frequencies. High-frequency representations remained tonotopic. Tonotopic asymmetries were independent of stimulus intensity. By contrast, in fluoro-2-deoxyglucose images from the same animals metabolic activity was tonotopically confined at high and low frequencies. The assymetric tonotopic propagation of ORIS activity suggests subthreshold directional interaction mechanisms in the cortical network which may serve to relate low- to high-frequency components of complex sounds.
The present study is concerned with conditioned reflex changes in background and evoked activity of the neuronal population of the auditory cortex (AI) in three waking cats. For the elaboration of a conditioned blink reflex, a series of eight clicks was used as the signal. The unconditional stimulus was rhythmic blowing of air at the eye. During the elaboration of a positive conditioned reflex there was a significant increase in the level of background activity. During conditioned reflex extinction, background activity showed a further increase. When extinguishing inhibition became profound, it was equivalent to sleep, and there was a strong fall in the level of background activity. During the restoration of an extinguished conditioned reflex, background activity fell to the level observed during conditioned reflex extinction, at the stage of consolidation. Application of an acoustic stimulus elicited a general, sometimes a slight increase in the number of spike discharges. Within the range of 300-350 ms - the time of appearance of the evoked response - neuronal activity underwent a reorganization, sometimes with a tendency to phasic variations. Phasic variations of the given population in response to sound were observed at all stages of the study.
The aim of this study was to measure and quantify habituation effects to auditory stimulation within the auditory cortex of 11 depressed patients with major depressive disorder compared to 11 healthy subjects. Habituation was visualized by functional magnetic resonance imaging (fMRI) employing a block design (repeated stimulation with sine tones). A subgroup of patients (n = 5) presented the following abnormal habituation fMRI pattern: significantly lower activation after the first stimulation block (p = 0.05), missing characteristic signal decay to repeated acoustic stimulation and a marked undershoot after each stimulation block. This abnormal pattern may indicate functional deficits in auditory processing occurring with depression, but our results need be confirmed in a larger, more homogeneous patient group. This paradigm may be a useful tool for assessing cortical dysfunction in mood disorders.
1. Responses of single units and multiunit clusters were recorded in the ferret primary auditory cortex (AI) with the use of broadband complex dynamic spectra. Previous work has demonstrated that simpler spectra consisting of single moving ripples (i.e., sinusoidally modulated spectral profiles that travel at a constant velocity along the logarithmic frequency axis) could be used effectively to characterize the response fields and transfer functions of AI cells. 2. A complex dynamic spectral profile can be thought of as being the sum of moving ripple spectra. Such a decomposition can be computed from a two-dimensional spectrotemporal Fourier transform of the dynamic spectral profile with moving ripples as the basis function. 3. Therefore, if AI units were essentially linear, satisfying the superposition principle, then their responses to arbitrary dynamic spectra could be predicted from the responses to single moving ripples, i.e., from the units' response fields and transfer functions (spectral and temporal impulse response functions, respectively). 4. This conjecture was tested and confirmed with data from 293 combinations of moving ripples, involving complex spectra composed of up to 15 moving ripples of different ripple frequencies and velocities. For each case, response predictions based on the unit transfer functions were compared with measured responses. The correlation between predicted and measured responses was found to be consistently high (84% with rho > 0.6). 5. The distribution of response parameters suggests that AI cells may encode the profile of a dynamic spectrum by performing a multiscale spectrotemporal decomposition of the dynamic spectral profile in a largely linear manner.
Recognition of sound patterns must be largely independent of level and of masking or jamming background sounds. Auditory patterns of relevance in numerous environmental sounds, species-specific vocalizations and speech are frequency modulations (FM). Level-dependent activation of the human auditory cortex (AC) in response to a large set of upward and downward FM tones was studied with low-noise (48 dB) functional magnetic resonance imaging at 3 Tesla. Separate analysis in four territories of AC was performed in each individual brain using a combination of anatomical landmarks and spatial activation criteria for their distinction. Activation of territory T1b (including primary AC) showed the most robust level dependence over the large range of 48-102 dB in terms of activated volume and blood oxygen level dependent contrast (BOLD) signal intensity. The left nonprimary territory T2 also showed a good correlation of level with activated volume but, in contrast to T1b, not with BOLD signal intensity. These findings are compatible with level coding mechanisms observed in animal AC. A systematic increase of activation with level was not observed for T1a (anterior of Heschl's gyrus) and T3 (on the planum temporale). Thus these areas might not be specifically involved in processing of the overall intensity of FM. The rostral territory T1a of the left hemisphere exhibited highest activation when the FM sound level fell 12 dB below scanner noise. This supports the previously suggested special involvement of this territory in foreground-background decomposition tasks. Overall, AC of the left hemisphere showed a stronger level-dependence of signal intensity and activated volume than the right hemisphere. But any side differences of signal intensity at given levels were lateralized to right AC. This might point to an involvement of the right hemisphere in more specific aspects of FM processing than level coding.