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Unit responses of the auditory cortex of waking cats at rest and after defensive conditioning.

In chronic experiments with glass microelectrodes responses of 288 spontaneously active neurons in the auditory cortex were investigated in cats at rest (123 neurons) and after defensive conditioning to sound (165 neurons). In the first situation 43% of neurons did not respond to acoustic stimulation. Most (about 60%) responses of the reacting neurons showed marked inhibition. Conditioning caused an increase (up to 72%) in the number of neurons responding to acoustic stimulation, the appearance of tonic responses, a severalfold increase in the amplitude of the responses, an increase in the number of responses of activation type, and stabilization of their form. The results point to increased excitability of neurons in this cortical area.

Animals↗

Antidromic activation reveals tonotopically organized projections from primary auditory cortex to the central nucleus of the inferior colliculus in guinea pig.

The inferior colliculus (IC) is highly modulated by descending projections from higher auditory and nonauditory centers. Traditionally, corticofugal fibers were believed to project mainly to the extralemniscal IC regions. However, there is some anatomical evidence suggesting that a substantial number of fibers from the primary auditory cortex (A1) project into the IC central nucleus (ICC) and appear to be tonotopically organized. In this study, we used antidromic stimulation combined with other electrophysiological techniques to further investigate the spatial organization of descending fibers from A1 to the ICC in ketamine-anesthetized guinea pigs. Based on our findings, corticofugal fibers originate predominantly from layer V of A1, are amply scattered throughout the ICC and only project to ICC neurons with a similar best frequency (BF). This strict tonotopic pattern suggests that these corticofugal projections are involved with modulating spectral features of sound. Along the isofrequency dimension of the ICC, there appears to be some differences in projection patterns that depend on BF region and possibly isofrequency location within A1 and may be indicative of different descending coding strategies. Furthermore, the success of the antidromic stimulation method in our study demonstrates that it can be used to investigate some of the functional properties associated with corticofugal projections to the ICC as well as to other regions (e.g., medial geniculate body, cochlear nucleus). Such a method can address some of the limitations with current anatomical techniques for studying the auditory corticofugal system.

Acoustic Stimulation↗

Representation of the voice onset time (VOT) speech parameter in population responses within primary auditory cortex of the awake monkey.

Voice onset time (VOT) signifies the interval between consonant onset and the start of rhythmic vocal-cord vibrations. Differential perception of consonants such as /d/ and /t/ is categorical in American English, with the boundary generally lying at a VOT of 20-40 ms. This study tests whether previously identified response patterns that differentially reflect VOT are maintained in large-scale population activity within primary auditory cortex (A1) of the awake monkey. Multiunit activity and current source density patterns evoked by the syllables /da/ and /ta/ with variable VOTs are examined. Neural representation is determined by the tonotopic organization. Differential response patterns are restricted to lower best-frequency regions. Response peaks time-locked to both consonant and voicing onsets are observed for syllables with a 40- and 60-ms VOT, whereas syllables with a 0- and 20-ms VOT evoke a single response time-locked only to consonant onset. Duration of aspiration noise is represented in higher best-frequency regions. Representation of VOT and aspiration noise in discrete tonotopic areas of A1 suggest that integration of these phonetic cues occurs in secondary areas of auditory cortex. Findings are consistent with the evolving concept that complex stimuli are encoded by synchronized activity in large-scale neuronal ensembles.

Animals↗

Modulation of the auditory cortex during speech: an MEG study.

Several behavioral and brain imaging studies have demonstrated a significant interaction between speech perception and speech production. In this study, auditory cortical responses to speech were examined during self-production and feedback alteration. Magnetic field recordings were obtained from both hemispheres in subjects who spoke while hearing controlled acoustic versions of their speech feedback via earphones. These responses were compared to recordings made while subjects listened to a tape playback of their production. The amplitude of tape playback was adjusted to match the amplitude of self-produced speech. Recordings of evoked responses to both self-produced and tape-recorded speech were obtained free of movement-related artifacts. Responses to self-produced speech were weaker than were responses to tape-recorded speech. Responses to tones were also weaker during speech production, when compared with responses to tones recorded in the presence of speech from tape playback. However, responses evoked by gated noise stimuli did not differ for recordings made during self-produced speech versus recordings made during tape-recorded speech playback. These data suggest that during speech production, the auditory cortex (1) attenuates its sensitivity and (2) modulates its activity as a function of the expected acoustic feedback.

Adult↗

Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex.

Acetylcholine (ACh), acting via muscarinic receptors, is known to modulate neuronal responsiveness in primary sensory neocortex. The administration of ACh to cortical neurons facilitates or suppresses responses to sensory stimuli, and these effects can endure well beyond the period of ACh application. In the present study, we sought to determine whether ACh produces a general change in sensory information processing, or whether it can specifically alter the processing of sensory stimuli with which it was "paired". To answer this question, we restricted acoustic stimulation in the presence of ACh to a single frequency, and determined single neuron frequency receptive fields in primary auditory cortex before and after this pairing. During its administration, ACh produced mostly facilitatory effects on spontaneous activity and on responses to the single frequency tone. Examination of frequency receptive fields after ACh administration revealed receptive field modifications in 56% of the cells. In half of these cases, the receptive field alterations were highly specific to the frequency of the tone previously paired with ACh. Thus ACh can produce stimulus-specific modulation of auditory information processing. An additional and unexpected finding was that the type of modulation during ACh administration did not predict the type of receptive field modulation observed after ACh administration; this may be related to the physiological "context" of the same stimulus in two different conditions. The implications of these findings for learning-induced plasticity in the auditory cortex is discussed.

Acetylcholine↗

Effects of primary auditory cortex lesions on middle latency responses in awake cats.

In order to clarify the role of the primary auditory cortex (AI) on middle latency responses (MLRs), we recorded the auditory evoked potentials (AEPs) from the vertex and the right and left AI areas of the skull simultaneously before and after creating serial lesions of the AIs contralateral and ipsilateral to the stimulated ear in 7 awake cats. The auditory brainstem responses (ABRs) and MLRs recorded from the vertex in normal awake cats revealed the presence of peaks 1-8, NA and PA within the analysis time of 50 msec. After there were serial AI lesions, (1) all the peaks remained at nearly the same latencies, (2) the amplitude of the NA was decreased significantly, that of the PA was slightly decreased and those of peaks 6, 7 and 8 were variable, and (3) the difference between the effects of the first operation (contralateral AI) and the second operation (ipsilateral AI) was not statistically significant. These findings indicated that the main, prominent effect of bilateral AI lesions on MLRs in the awake cat is a significant decrease in the NA amplitude.

Anesthesia, General↗

Neuronal mechanisms of auditory backward recognition masking in macaque auditory cortex.

The sensation of a single sound event can be altered by subsequent sounds. This study searched for neural mechanisms of such retroactive effects in macaque auditory cortex by comparing neural responses to single tones with responses to two consecutive tones. Retroactive influences were found to affect late parts of the response to a tone, which comprised 53/134 of the recordings of action potentials and 88/131 of the recordings of field potentials performed in primary, caudal, and medial auditory fields. If before or during the occurrence of the late response to the first tone a second tone was presented the late response was suppressed. Suppression of late cortical responses parallels perceptual phenomena like backward recognition masking, suggesting that suppression of late responses provides a neural correlate of auditory backward effects.

Acoustic Stimulation↗

Tonotopic organization of the human auditory cortex: N100 topography and multiple dipole model analysis.

The tonotopic organization of the human auditory cortex has been investigated by means of scalp potential mapping and dipole modelling of the evoked response occurring around 100 msec after the stimulus onset. The major characteristics of the topographical changes observed with increasing stimulus frequency were statistically demonstrated. Using a 3-concentric sphere head model, the scalp potential distributions can be explained in first approximation by two equivalent current dipoles, located in the supratemporal plane and mimicking the activity of both auditory cortices. To take into account the temporal aspects of the brain activities, 3 time-varying dipole strategies were tested. Frequency dependence of the dipole orientation has been evidenced in both hemispheres with the 3 models, whereas no significant change in dipole position was found. The tilt in dipole orientation could be related to the folding geometry of Heschl's gyrus, which varies with depth. In agreement with previous MEG findings, this brings new evidence for a tonotopic organization of the auditory cortical area involved in the N100 wave generation. Moreover, distinct frequency dependences of the equivalent current dipoles were observed in the early and the late parts of the N100. This study demonstrates that simple dipolar models, applied on electrical data, make it possible to reveal functionally distinct cortical areas.

Adult↗

Distribution and kinetic properties of GABAergic inputs to layer V pyramidal cells in rat auditory cortex.

Neocortical layer V is distinguished by both its pyramidal cells and its varied cortical and extracortical projections. Several studies suggest that the layer V pyramidal cell types, intrinsically bursting (IB) and regular spiking (RS) cells, differ both in the circuits in which they participate and in their inhibitory inputs. We quantified differences in inhibitory inputs to RS and IB cells using whole-cell voltage clamp techniques in the auditory cortex. We recorded miniature inhibitory postsynaptic currents (mIPSCs) and spontaneous IPSCs to gain kinetic, amplitude, and frequency information about GABAergic synapses. We then used focal sucrose applications to elicit mIPSC rate increases at the soma or dendrites of both cell types. We also electrically stimulated the axons giving rise to inhibitory synaptic inputs to measure minimally evoked IPSCs occurring at the soma or apical dendrites. We found that spontaneous and evoked IPSCs recorded from the auditory cortex have faster rise and decay kinetics when directly compared with those of the same layer V cells in other sensory cortical areas. We also found that mIPSCs observed in auditory IB and RS cells are different from one another. RS cell mIPSCs are larger and have faster rises and decays than IB cell mIPSCs, but IB cell mIPSCs occur more frequently. Focal sucrose application showed that most IB cell mIPSCs originate in the dendrites and are subject to dendritic filtering while most RS cell mIPSCs originate at the soma and are not filtered. These findings suggest that, first, IB and RS cells process their inputs in fundamentally different ways and, second, auditory cortical RS and IB cells may have specializations that allow them to process inhibitory inputs faster.

Animals↗

Injury-induced reorganization of frequency maps in adult auditory cortex: the role of unmasking of normally-inhibited inputs.

Restricted cochlear lesions in adult animals, causing partial deafness, result in a reorganization of primary auditory cortex (AI) such that the region deprived of its normal input by the lesion is occupied by an expanded representation of peri-lesion cochlear regions, and hence of peri-lesion frequencies. One possible mechanism underlying the change in frequency responsiveness involved in such reorganization is that inputs to the cortical neurons at frequencies at and near their "new" post-lesion characteristic frequencies (CFs) are normally present but suppressed by inhibition, and are "unmasked" by the effects of the lesion. Evidence in support of this explanation is provided by two-tone forward-masking experiments which reveal that many AI neurons receive surround inhibitory input. When input to such neurons at their CF is reduced by an intense temporary-threshold-shift (TTS)-inducing stimulus, the response areas of some neurons expand into the region of their inhibitory surrounds, the effect that would be expected if unmasking were involved in cortical reorganization. In other neurons, however, response areas contracted after the TTS-inducing stimulation. Although unmasking of normally-inhibited inputs is likely to contribute to auditory cortical reorganization, the immediate unmasking that is seen in visual and somatosensory systems is unlikely to play a major role in auditory cortical reorganization, as no evidence of immediate unmasking was seen following acute cochlear lesions in guinea pigs.

Animals↗

Short-term functional plasticity in the human auditory cortex: an fMRI study.

Applying functional magnetic resonance imaging (fMRI) techniques, hemodynamic responses elicited by sequences of pure tones of 950 Hz (standard) and deviant tones of 952, 954, and 958 Hz were measured before and 1 week after subjects had been trained at frequency discrimination for five sessions (over 1 week) using an oddball procedure. The task of the subject was to detect deviants differing from the standard stimulus. Frequency discrimination improved during the training session for three subjects (performance gain: T+) but not for three other subjects (no performance gain: T-). Hemodynamic responses in the auditory cortex comprising the planum temporale, planum polare and sulcus temporalis superior significantly decreased during training only for the T+ group. These activation changes were strongest for those stimuli accompanied by the strongest performance gain (958 and 954 Hz). There was no difference with respect to the hemodynamic responses in the auditory cortex for the T- group and the control group (CO) who did not received any pitch discrimination training. The results suggest a plastic reorganization of the cortical representation for the trained frequencies which can be best explained on the basis of 'fast learning' theories.

Acoustic Stimulation↗

Spectrotemporal features of the auditory cortex: the activation in response to dynamic ripples.

Functional MRI was used to investigate the characteristics of the human cerebral response to dynamic ripples. Dynamic ripples are sound stimuli containing regular spectrotemporal modulations, which are of major importance in speech processing; however, in contrast to speech, dynamic ripples can be characterized fully by a limited number of parameters. Extensive activation consisting of multiple separate regions was found bilaterally in the auditory cortex, particularly along the Heschl's gyri. This agrees with the presence of a structural cortical subdivision into functional fields. The level and the extent of activation were measured and correlated highly (R(2) = 0.97). Both measures depended strongly on the spectral density, temporal frequency, and amplitude of the modulations and matched the perceptual discernibility of the spectrotemporal modulations. The largest responses occurred for parameter values near the optimal human sensitivity. The drift direction of the modulations did not influence the activation. No quantitative differences were found between the two hemispheres. Average brain activation levels proved to be separable with regard to the spectral density and temporal frequency of the modulations. Topographic mappings of the modulation density and frequency onto the cortical surface were shown, approximately in posterolateral-to-anteromedial and lateral-to-medial directions, respectively. Posterolateral regions were most sensitive to spectrotemporal features at a scale similar to phonemes. Anteromedial regions, however, were also relatively sensitive to smaller scale acoustic features. This spatially dependent sensitivity suggests a functional topographic and hierarchical organization of the auditory cortex.

Acoustic Stimulation↗

Single unit activity in the auditory cortex of a monkey performing a short term memory task.

Short term memory to tones (STMT) was investigated by recording single unit activity in the auditory cortex of a behaving monkey. The activity of each unit was studied in two behavioral conditions: a) During task performance, the monkey had to compare two tones separated by one second of silence (inter-stimulus interval). b) During a non-performing period; the monkey heard the two tones but did not respond behaviorally. It was noted that the firing rate of many units during the inter-stimulus interval (ISI) was dependent on the frequency of the first tone. Such dependency was observed even towards the end of the ISI, both during task performance trials (50% of the units) and during the non-performing period (32% of the units). The activity of these units could be the basis of STMT in both of these behavioral states. In 65% of all the units tested, the responses during the ISI were of a higher magnitude in the performance period than were the responses in the non-performance period. The activity of these units may be related either to general processes such as attention and expectation or to short-term memory processes. During task performance, the responses of 23% of the units to the second tone were dependent on whether its frequency was identical to that of the first tone. Such dependency was never observed during the non-performing period. These units may detect similarity or non similarity between two tones presented one second apart. Periodic patterns of firing were not found in the study, thus suggesting that the ISI responses were not generated by reverberatory activity in simple closed loops. On the basis of these results, several alternative mechanisms of STMT are suggested.

Acoustic Stimulation↗

The morphometry of auditory cortex in the congenitally deaf measured using MRI.

The study of congenitally deaf individuals provides a unique opportunity to understand the organization and potential for reorganization of human auditory cortex. We used magnetic resonance imaging (MRI) to examine the structural organization of two auditory cortical regions, Heschl's gyrus (HG) and the planum temporale (PT), in deaf and hearing subjects. The results show preservation of cortical volume in HG and PT of deaf subjects deprived of auditory input since birth. Measurements of grey and white matter, as well as the location and extent of these regions in the deaf showed complete overlap both with matched controls and with previous samples of hearing subjects. The results of the manual volume measures were supported by findings from voxel-based morphometry analyses that showed increased grey-matter density in the left motor hand area of the deaf, but no differences between the groups in any auditory cortical region. This increased cortical density in motor cortex may be related to more active use of the dominant hand in signed languages. Most importantly, expected interhemispheric asymmetries in HG and PT thought to be related to auditory language processing were preserved in these deaf subjects. These findings suggest a strong genetic component in the development and maintenance of auditory cortical asymmetries that does not depend on auditory language experience. Preservation of cortical volume in the deaf suggests plasticity in the input and output of auditory cortex that could include language-specific or more general-purpose information from other sensory modalities.

Adult↗

Ultrasound activates the auditory cortex of profoundly deaf subjects.

Using three-dimensional PET, the cortical areas activated by bone-conducted ultrasound were measured from five profoundly deaf subjects and compared with the cortical areas of normal-hearing subjects activated by stimuli through bone-conducted ultrasonic, air-conducted, bone-conducted, and vibro-tactile hearing aids. All of the hearing aids, including the ultrasonic hearing aid, consistently activated the medial portion of the primary auditory cortex of the normal volunteers. The same cortical area was also significantly activated in the profoundly deaf subjects although the percentage increase in regional cerebral blood flow (rCBF) was smaller than in normal subjects. These results suggest that extra-cochlear routes convey information to the primary auditory cortex and can therefore produce detectable sound sensation even in the profoundly deaf subjects, who reported a sensation themselves.

Adult↗

Organization of auditory cortex in the owl monkey (Aotus trivirgatus).

The region of cerebral cortex in the owl monkey that is responsive to acoustic stimulation is located on the dorsal and lateral surfaces of the rostral half of the superior temporal gyrus. Systematic microelectrode mapping of this area has revealed multiple frequency representations. The boundaries of these fields determined electrophysiologically correlate with the architectural boundaries apparent in Nissl stained material. On the basis of combined cytoarchitectonic and electrophysiological maps we have divided auditory cortex into five fields. Two of them, the primary field (AI) and the field rostral to it (R) are somewhat similar architectonically and constitute the central core of auditory cortex. Each of these two fields has a complete and orderly representation of the audible frequency spectrum within it. Surrounding these fields is a belt of cortex in which units are generally less responsive to acoustic stimulation and the frequency organization is more complex than in AI or R. Electrophysiological and cytoarchitectonic evidence suggest that this belt is composed of at least three and possibly four separate auditory fields.

Acoustic Stimulation↗

Functional organization of the auditory cortex in a native Chilean rodent (Octodon degus).

The tonotopic organization of primary auditory cortex (AI) and surrounding secondary regions has been studied in the Octodon degus using standard microelectrode mapping techniques. The results confirm and extend previous observations made in other species. The tonotopic organization of the largest field (AI) apparently covered the hearing range of O. degus. Low tonal frequencies were represented rostroventrally and high frequencies caudally, with isofrequency contours orientated dorsoventrally in a ventrocaudal slant. There were additional tonotopic representations adjacent to AI. Rostral to AI, a small field with a tonotopic gradient reversed with respect to that in AI (mirror image representation) was mapped and termed rostral auditory field (R). Best frequencies (BF's) in a range from 0.1-30.0 kHz were found in AI and R, with higher spatial resolution for the representation of lower BF's up to 10.0 kHz. Responses obtained in AI as well as in R were strong, with narrow tuning and short latencies. Caudal to AI, two small additional, tonotopically organized fields, the dorsoposterior field (DP) and the ventroposterior field (VP), could be distinguished. In fields VP and DP, high BF's were situated rostrally, adjacent to the high frequency representation in AI. Low frequency representations were found in caudal part of DP and VP fields. Responses to tone burst within DP and VP were mostly weak, with longer latencies and broader tuning compared to those found in AI and R.

Acoustic Stimulation↗

GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium binding proteins and surface antigens.

The primary auditory cortex (A1) of monkeys was investigated by immunohistochemistry, using antibodies to gamma-aminobutyric acid (GABA), to the calcium binding proteins parvalbumin and calbindin, and to certain proteoglycan epitopes. The two calcium binding proteins were found to be localized in subpopulations of GABAergic neurons. Parvalbumin immunoreactive cells were mostly found in the middle layers of the cortex. Parvalbumin immunoreactivity was found in fibres in the white matter underlying A1 and a particularly dense concentration of parvalbumin immunoreactive fibers and terminals occurred in layer IV suggesting that a significant population of geniculocortical fibers is also parvalbumin positive. Calbindin positive cells were mostly located in superficial layers and in these layers the neuropil staining was also dense. Two monoclonal antibodies (MAbs) raised against monkey brain tissue and which had previously been shown to recognize neuronal surface antigens stained overlapping subpopulations of GABAergic cells. Occasional pyramidal cells were also immunoreactive. Most of the MAb positive cells were found in the middle layers and all were parvalbumin but not calbindin immunoreactive. Although the physiological roles in the brain for calcium binding proteins and the relevant cell surface markers have not yet been clarified, the presence of these markers in selected subpopulations of cells suggests the existence of functionally distinct circuits in AI cortex.

Animals↗