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Level-dependent representation of stimulus frequency in cat primary auditory cortex.

The tonotopicity of the cat's primary auditory cortex (AI) is thought to provide the framework for frequency-specific processing in that field. This study was designed to assess this postulate by examining the spatial distribution of neurons within AI that are activated by a single tonal frequency delivered to the contralateral ear. Distributions obtained at each of several stimulus levels were then compared to assess the influence of stimulus amplitude on the spatial representation of a given stimulus frequency in AI. Data were obtained from 308 single units in AI of four adult, barbiturate-anesthetized cats, using extracellular recording methods. Stimuli were 40-ms tone pulses presented through calibrated, sealed stimulating systems. In each animal, the CF (stimulus frequency to which the unit is most sensitive), threshold at CF, response/level function at CF, and binaural interactions were determined for isolated neurons (usually one per track) in 60-90 electrode tracks. For each unit, regardless of its CF, responses to 40 repetitions of contralateral tones of a single frequency, presented at each of four or five sound pressure levels (SPLs) in the range from 10 to 80 dB were obtained. Different test frequencies were used in each of four cats (1.6, 8.0, 11.0, and 16.0 kHz). For tones of each SPL, we generated maps of the response rates across the cortical surface. These maps were then superimposed on the more traditional maps of threshold CF. All units whose CF was equal to the test frequency could be driven at some SPL, given an appropriate monaural or binaural configuration of the stimulus. There was a clear spatial segregation of neurons according to the shapes of their CF tone response/level functions. Patches of cortex, often occupying more than 2 mm2, seemed to contain only monotonic or only nonmonotonic units. In three cortices, a patch of nonmonotonic cells was bounded ventrally by a patch of monotonic cells, and in one of these cases, a second patch of monotonic cells was found dorsal to the nonmonotonic patch. Contralateral tones of any given SPL evoked excitatory responses in discontinuous cortical territories. At low SPLs (10, 20 dB), small foci of activity occurred along the isofrequency line representing the test frequency. Many of these cells had nonmonotonic response/level functions. (ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Regional response differences within the human auditory cortex when listening to words.

The relationship between activity within the human auditory cortices and the presentation rate of heard words was investigated by measuring changes in regional cerebral blood flow with positron emission tomography. We demonstrate that in the primary auditory cortices and middle regions of the superior temporal gyri there is a linear relationship between the rate of presentation of heard words and blood flow response. In contrast, the blood flow response in an area of the left posterior superior temporal gyrus (Wernicke's area) is primarily dependent on the occurrence of words irrespective of their rate of presentation. The primary auditory cortices are associated with the early processing of complex acoustic signals whereas Wernicke's area is associated with the comprehension of heard words. This study demonstrates for the first time that time dependent sensory signals (heard words) detected in the primary auditory cortices are transformed into a time invariant output which is channelled to a functionally specialised region--Wernicke's area. Wernicke's area is therefore distinguished from other areas of the auditory cortex by direct observation of signal transformation rather than by association with a specific behavioural task.

Adult↗

Unilateral auditory cortex ablation in macaques results in a contralateral hearing loss.

1. The behavioral audiograms of four Japanese macaques (Macaca fuscata) were assessed before and after unilateral ablation of auditory cortex. The tones were presented via insertion earphones so that each ear could be tested separately. 2. Each animal had a hearing loss in the ear contralateral to the lesion, whereas the ipsilateral ear showed no change in sensitivity. The hearing loss initially appeared as a large shift in thresholds followed by rapid but incomplete recovery during the first 3-5 wk after surgery. The initial hearing loss ranged as high as 68 dB at some frequencies, although thresholds at other frequencies were occasionally unchanged. A threshold shift could be demonstrated with broadband noise as well as with tones. Although thresholds for some tones returned to normal within a few weeks, most were still elevated 16 wk after surgery when testing was discontinued. The largest long-term hearing losses occurred at frequencies from 4 to 25 kHz. 3. Analysis of the animals' psychophysical functions suggested that the hearing loss resembled a sensory deficit, as opposed to a nonsensory deficit in attention or vigilance. 4. Testing with binaural stimuli indicated that the hearing loss could best be described as a contralateral "ear" deficit, as opposed to a contralateral "auditory field" deficit. 5. It is suggested that a similar hearing loss occurs in humans after unilateral damage to auditory cortex.

Animals↗

Importance of polysynaptic inputs and horizontal connectivity in the generation of tetanus-induced long-term potentiation in the rat auditory cortex.

Supragranular pyramidal neurons in the adult rat auditory cortex (AC) show marked long-term potentiation (LTP) of population spikes after tetanic white matter stimulation (TS). For determination of whether this marked LTP is specific to AC, LTP in rat AC slices was compared with LTP in slices of the visual cortex (VC). The amplitude of TS-induced LTP in AC was twice that in VC. LTP of EPSPs was also studied with perforated patch or whole-cell recording. Although the amplitude of TS-induced LTP of EPSPs in AC was larger that in VC, no cortical difference was found in LTP elicited by low-frequency stimulation paired with current injection. Neocortical LTP is dependent on the activation of NMDA receptors, and induction of LTP requires postsynaptic depolarization for removal of Mg2+ blockade of NMDA receptors. The postsynaptic depolarization elicited by TS in supragranular pyramidal neurons in AC was significantly larger than that in VC. Cutting of supragranular horizontal connections resulted in a decrease in the depolarization amplitude in AC but an increase in the depolarization amplitude in VC. The cortical difference in TS-induced LTP was diminished in the slices in which horizontal connections in supragranular layers were cut. The estimated density of horizontal axon collaterals of supragranular pyramidal neurons in AC was approximately twice that in VC. These results strongly suggest that the marked polysynaptic and postsynaptic depolarization during TS and the resulting marked LTP in AC are attributed to well developed horizontal axon collaterals of supragranular pyramidal neurons in AC.

2-Amino-5-phosphonovalerate↗

Short-term sound temporal envelope characteristics determine multisecond time patterns of activity in human auditory cortex as shown by fMRI.

Functional magnetic resonance imaging (fMRI) of human auditory cortex has demonstrated a striking range of temporal waveshapes in responses to sound. Prolonged (30 s) low-rate (2/s) noise burst trains elicit "sustained" responses, whereas high-rate (35/s) trains elicit "phasic" responses with peaks just after train onset and offset. As a step toward understanding the significance of these responses for auditory processing, the present fMRI study sought to resolve exactly which features of sound determine cortical response waveshape. The results indicate that sound temporal envelope characteristics, but not sound level or bandwidth, strongly influence response waveshapes, and thus the underlying time patterns of neural activity. The results show that sensitivity to sound temporal envelope holds in both primary and nonprimary cortical areas, but nonprimary areas show more pronounced phasic responses for some types of stimuli (higher-rate trains, continuous noise), indicating more prominent neural activity at sound onset and offset. It has been hypothesized that the neural activity underlying the onset and offset peaks reflects the beginning and end of auditory perceptual events. The present data support this idea because sound temporal envelope, the sound characteristic that most strongly influences whether fMRI responses are phasic, also strongly influences whether successive stimuli (e.g., the bursts of a train) are perceptually grouped into a single auditory event. Thus fMRI waveshape may provide a window onto neural activity patterns that reflect the segmentation of our auditory environment into distinct, meaningful events.

Acoustic Stimulation↗

Spect-studies of the brain with stimulation of the auditory cortex.

The radiopharmaceutical N-isopropyl-p-J-Amphetamin (IMP) permits a new approach in the study of cerebral perfusion and function. We advanced the hypothesis for an increased IMP-uptake on auditory cortex during stimulation by white noise. Auditory stimulation activates the auditory cortex. This is marked by an increased IMP-uptake. IMP-uptake by the auditory region on the left side during stimulation on the right ear is another evidence of the crossing of central auditory pathways to the contralateral side.

Acoustic Stimulation↗

Long-term retention of learning-induced receptive-field plasticity in the auditory cortex.

Brief learning experience (classical conditioning) induces frequency-specific receptive-field (RF) plasticity in the auditory cortex, characterized as increased response to the frequency of the conditioned stimulus and decreased responses to most other frequencies, including the pretraining best frequency. This experiment asked (i) whether learning-induced RF plasticity, established in the waking state, can be expressed under general anesthesia and if so (ii) whether it exhibits long-term retention. Pure-tone-frequency RFs were obtained from adult guinea pigs under general anesthesia (sodium pentobarbital or ketamine) before and repeatedly after (1 hr-8 weeks) a 20- to 30-trial session of pairing a non-best-frequency tone with mild footshock. Conditioned-stimulus-specific RF plasticity was expressed under both types of anesthesia and included shifts of the pretraining best frequency toward or even to the frequency of the conditioned stimulus. Moreover, this RF plasticity exhibits long-term retention, being evident 1-8 weeks after training. This satisfies a criterion for the long-term storage of information in the auditory cortex.

Acoustic Stimulation↗

Intrinsic organization of the cat's medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex.

The area of the cat's primary auditory cortex (AI) within which high frequency sounds are represented can be subdivided using functional criteria. Within each subdivision, or "binaural interaction band," all recorded neurons display similar responses to binaural stimulation. The current study distinguishes the thalamic sources of input to these subdivisions of AI and characterizes the topography within the thalamic projection to each class of bands. The borders of binaural bands in AI were mapped using microelectrode recording with diotic tonal stimulation, then injections of one to three retrograde tracers were introduced into identified bands. Within the ventral division (V) of the medial geniculate body (the major thalamic source of input to AI), the neuronal populations that projected to different classes of binaural bands were strictly segregated from each other. This segregation of class-specific thalamic sources constitutes a laminar organization within an axis of V that is orthogonal to the previously described tonotopic organization. Excitatory/excitatory (EE) binaural neurons in AI were found to be segregated from excitatory/inhibitory (EI) neurons in alternating "bands." We consistently identified: (1) a ventral pair of rostrocaudally continuous EI and EE bands, (2) a middle area within which the pattern of binaural subdivisions was more variable and within which bands often were discontinuous rostrocaudally, and (3) a dorsal zone (DZ) within which the responses of neurons differed in binaural properties and in frequency specificity from the response patterns that were characteristic of neurons elsewhere in AI. Each EI band apparently derived input that converged from three thickened laminae of cells in V that were oriented approximately horizontally. The most ventral of these laminae encompassed the ovoidal part of V (Vo), suggesting that EI bands are the only recipients in AI of a projection from Vo. All of the EE bands and DZ derived their input from a single continuous structure which included the dorsal two-thirds of the rostral pole of V and a horizontal lamina interposed between the two dorsalmost EI-projecting laminae. Restricted portions of the complex EE-projecting structure in V projected preferentially to particular EE subdivisions of AI. The V-to-AI thalamocortical topography exhibited a high degree of convergence and divergence within the projections to each cortical binaural band and within the projections to each class of bands. These observations indicate that the high frequency representation in AI and its principal thalamic source of input, the ventral division of the medial geniculate body, may be thought of as assemblies of spatially discrete, functionally distinguishable subunits. The significance of this intrinsic organization is discussed in regard to the requirements for analysis of sound stimuli.

Animals↗

Modular organization of frequency integration in primary auditory cortex.

Two fundamental aspects of frequency analysis shape the functional organization of primary auditory cortex. For one, the decomposition of complex sounds into different frequency components is reflected in the tonotopic organization of auditory cortical fields. Second, recent findings suggest that this decomposition is carried out in parallel for a wide range of frequency resolutions by neurons with frequency receptive fields of different sizes (bandwidths). A systematic representation of the range of frequency resolution and, equivalently, spectral integration shapes the functional organization of the iso-frequency domain. Distinct subregions, or "modules," along the iso-frequency domain can be demonstrated with various measures of spectral integration, including pure-tone tuning curves, noise masking, and electrical cochlear stimulation. This modularity in the representation of spectral integration is expressed by intrinsic cortical connections. This organization has implications for our understanding of psychophysical spectral integration measures such as the critical band and general cortical coding strategies.

Animals↗

Lack of cortico-striatal projections from the primary auditory cortex in the squirrel monkey.

The projections of the superior temporal gyrus to the caudate nucleus were studied in 10 squirrel monkeys (Saimiri sciureus). It was found that the primary auditory cortex lacks direct connections with the caudate nucleus as well as the putamen. Areas RL and T1 of Burton and Jones, bordering the primary auditory cortex laterally, show a moderate projection to the body and tail of the caudate nucleus; area T2, bordering areas RL and T1, shows an extensive projection into the head, body and tail. A comparison of the temporo-caudate projections of the monkey with those of rodents and carnivores suggests that primary and secondary auditory cortices differ in their connections in primates more than in other mammals, pointing to a greater functional differentiation of these areas in primates.

Animals↗

Vowel processing evokes a large sustained response anterior to primary auditory cortex.

The present study uses electroencephalography (EEG) and a new stimulation paradigm, the 'continuous stimulation paradigm', to investigate the neural correlate of phonological processing in human auditory cortex. Evoked responses were recorded to stimuli consisting of a control sound (1000 ms) immediately followed by a test sound (150 ms). On half of the trials, the control sound was a noise and the test sound a vowel; to control for unavoidable effects of spectral change at the transition, the roles of the stimuli were reversed on the other half of the trials. The acoustical properties of the vowel and noise sounds were carefully matched to isolate the response specific to phonological processing. As the unspecific response to sound energy onset has subsided by the transition to the test sound, we hypothesized that the transition response from a noise to a vowel would reveal vowel-specific processing. Contrary to this expectation, however, the most striking difference between vowel and noise processing was a large, vertex-negative sustained response to the vowel control sound, which had a fast onset (30-50 ms) and remained constant throughout presentation of the vowel. The vowel-specific response was isolated using a subtraction technique analogous to that commonly applied in neuroimaging studies. This similarity in analysis methodology enabled close comparison of the EEG data collected in the present study with relevant functional magnetic resonance (fMRI) literature. Dipole source analysis revealed the vowel-specific component to be located anterior and inferior to primary auditory cortex, consistent with previous data investigating speech processing with fMRI.

Adult↗

Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat.

Focal excess sensory stimulation evokes reorganization of a sensory system. It is usually an expansion of the neural representation of that stimulus resulting from the shifts of the tuning curves (receptive fields) of neurons toward those of the stimulated neurons. The auditory cortex of the mustached bat has an area that is highly specialized for the processing of target-distance information carried by echo delays. In this area, however, reorganization is due to shifts of the delay-tuning curves of neurons away from those of the stimulated cortical neurons. Elimination of inhibition in the target-distance processing area in the auditory cortex by a drug reverses the direction of the shifts in neural tuning curves. Therefore, such unique reorganization in the time domain is due to strong lateral inhibition in the highly specialized area of the auditory cortex.

Acoustic Stimulation↗

Interlaminar differences of spike activation threshold in the auditory cortex of the rat.

The neural circuits of the auditory cortex are a substrate for the dual purpose of representing and storing the auditory signal on one hand, and sending its relevant features to other cortical and subcortical areas on the other hand. The ability to process and transform the signal crucially depends on achievement of the neuronal spike threshold following spatiotemporal summation of the synaptic signals. We used patch-clamp recording in a thin slice preparation to compare neuronal responses to current injection of layer II/III and layer V neurons. We found that while the two classes of neurons do not differ in passive neuronal properties, layer II/III neurons possess a lower firing threshold relative to layer V neurons (-44.8 +/- 2.4 mV vs. -34.3 +/- 4.0 mV). We speculate that a lower spiking threshold in layer II/III neurons might favor local intracolumnar activation for representation and storage of the auditory information whereas a more positive spiking threshold for layer V neurons may prevent unnecessary cortical spread of a scarcely processed signal.

Action Potentials↗

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

1. Because the ventroanterior (VA) area is one of the target areas of the FM-FM area in the auditory cortex of the mustached bat, Pteronotus parnellii parnellii, response properties of combination-sensitive neurons in this area were studied with constant-frequency (CF) tones, frequency-modulated (FM) sounds, and sounds similar to the bat's biosonar signal (pulse), which consisted of long CF components (CF1-4) and short FM components (FM1-4). CF1-4 and FM1-4 are the components in the four harmonics (H1-4) of the pulse. 2. Combination-sensitive neurons are clustered in a small area immediately anteroventral to the Doppler-shifted CF processing (DSCF) area and posteroventral to the anterior division of the primary auditory cortex. Because this cluster in the VA area is small, it was difficult to record a sufficient number of combination-sensitive neurons to explore the functional organization of the cluster, but it was found that the response properties of these VA neurons were unique. 3. Combination-sensitive neurons in the VA area are tuned to particular combinations of signal elements similar to the first and second harmonics of the pulse and/or echo. Unlike neurons in the FM-FM, dorsal fringe (DF), and CF/CF areas, no neurons in the VA area are tuned to the signal elements in the first and third or fourth harmonics. 4. The great majority of combination-sensitive neurons in the VA area can not be easily classified into either FM-FM or CF/CF neurons, because they show facilitative responses to combinations of CF1/CF2, FM1-FM2, and FM1-CF2. Therefore, they are called H1-H2 neurons. In the FM-FM and CF/CF areas, all the neurons could be easily classified as FM-FM or CF/CF. This uniqueness of H1-H2 neurons is related to the fact that their best frequencies for facilitation are predominantly between 61.0 and 62.0 kHz, i.e., within the frequency range of stabilized Doppler-shifted echo CF2. 5. In addition to 27 H1-H2 neurons, 7 FM1-FM2 neurons were also recorded in the VA area. The best delays of these H1-H2 and FM1-FM2 neurons measured with FM1-FM2 pairs are between 1 and 10 ms. Unlike neurons in the FM-FM and DF areas, their delay-tuning curves are very broad, even if their best delays are short, and extend beyond zero delay to several millisecond "negative" delays of the FM2 from the FM1, i.e., several millisecond delays of the FM1 from the FM2.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗

[Spreading excitation in the upper (I-III) layers of an isolated strip of cat auditory cortex].

Lower layers of the isolated slab in the auditory cortex were cut, one, two or three cortical layers under the pial surface remaining intact. Impulse reactions of neurons to the intracortical stimulation applied on the other side of this additional cut were investigated in acute experiments on unanaesthetized immobilized cats. It was shown that stimulation of layer IV generated a flow of excitation ascending to the upper cortical layers and activating mono- and polysynaptically neurons of all layers through the vertical bundles of apical dendrites of pyramidal cells. Suggestion is made about an important role a large bundle of axons of layer III plays in the horizontal spread of excitation in the cerebral cortex.

Animals↗

Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats.

To investigate possible cross-modal reorganization of the primary auditory cortex (field A1) in congenitally deaf cats, after years of auditory deprivation, multiunit activity and local field potentials were recorded in lightly anesthetized animals and compared with responses obtained in hearing cats. Local field potentials were also used for current source-density analyses. For visual stimulation, phase-reversal gratings of three to five different spatial frequencies and three to five different orientations were presented at the point of central vision. Peripheral visual field was tested using hand-held stimuli (light bar-shaped stimulus of different orientations, moved in different directions and flashed) typically used for neurophysiological characterization of visual fields. From 200 multiunit recordings, no response to visual stimuli could be found in A1 of any of the investigated animals. Using the current source-density analysis of local field potentials, no local generators of field potentials could be found within A1, despite of the presence of small local field potentials. No multiunit responses to somatosensory stimulation (whiskers, face, pinna, head, neck, all paws, back, tail) could be obtained. In conclusion, there were no indications for a cross-modal reorganization (visual, somatosensory) of area A1 in congenitally deaf cats.

Animals↗

[Connections between area AIV and areas AI, AII and Ep of the auditory cortex in the cat].

Zones AI A11 and Ep in the cat auditory corex have been studied layer-by-layer electron microscopically after the zone AIV has been removed. Terminals having degeneration signs according to the dark type are mainly found in the layers V-VI of all the auditory cortex zones studied. Additional degenerative zones are revealed in the layer I of the zone AII and in the layer II of the zone Ep. Not any additional foci of degeneration are found in the zone AI. A suggestion is made concerning a physiological significance of the afferent distribution in the connective systems investigated. The corticocortical connections are formed by axodendritic and axospine synapses.

Animals↗