The auditory cortex

The division of the auditory cortex into various fields, functional aspects of these fields, and neuronal coding in the primary auditory cortical field (AI) are reviewed with stress on features that may be common to mammals. On the basis of 14 topographies and clustered distributions of neuronal response characteristics in the primary auditory cortical field, a hypothesis is developed of how a certain complex acoustic pattern may be encoded in an equivalent spatial activity pattern in AI, generated by time-coordinated firing of groups of neurons. The auditory cortex, demonstrated specifically for AI, appears to perform sound analysis by synthesis, i.e. by combining spatially distributed coincident or time-coordinated neuronal responses. The dynamics of sounds and the plasticity of cortical responses are considered as a topic for research. Accepted: 25 July 1997     

Reaction of neurons of the medial geniculate body to acoustic stimulation

Responses of medial geniculate body (MGB) neurons to pure tones and clicks were studied in acute experiments in immobilized cats, preliminary operations being performed under calypsol anaesthesia. MGB units were identified by their reactions to cortical zone AI and brachium of inferior colliculus stimulations. When tonal stimuli were applied relay neurons of pars principalis of MGB usually demonstrated either unimodal tuning curves with narrow frequency band or fragmental ones with several narrow bands. On-response with subsequent inhibition of the background activity or without such an inhibitory period was most frequent type of the reaction (66.6%) of relay MGB neurons to tonal stimulation. The group of relay neurons with the tonic type of reaction (9.1%) was classified for which the duration of tonic response depends on the duration of tonal stimulus. Change of the excitatory reaction to the inhibitory one when the characteristic tone frequency is changed by non-characteristic++ ones is supposed to be a mechanism supplying sharpness of tuning at relay MGB neurons. It is concluded that responses of acoustic cortical neurons to sound stimulation depend to a great extent on the pattern of impulsation that comes from MGB relay units.     

Cortical Representation of Species-Specific Vocalizations in Guinea Pig

We investigated the representation of four typical guinea pig vocalizations in the auditory cortex (AI) in anesthetized guinea pigs with the aim to compare cortical data to the data already published for identical calls in subcortical structures - the inferior colliculus (IC) and medial geniculate body (MGB). Like the subcortical neurons also cortical neurons typically responded to many calls with a time-locked response to one or more temporal elements of the calls. The neuronal response patterns in the AI correlated well with the sound temporal envelope of chirp (an isolated short phrase), but correlated less well in the case of chutter and whistle (longer calls) or purr (a call with a fast repetition rate of phrases). Neuronal rate vs. characteristic frequency profiles provided only a coarse representation of the calls’ frequency spectra. A comparison between the activity in the AI and those of subcortical structures showed a different transformation of the neuronal response patterns from the IC to the AI for individual calls: i) while the temporal representation of chirp remained unchanged, the representations of whistle and chutter were transformed at the thalamic level and the response to purr at the cortical level; ii) for the wideband calls (whistle, chirp) the rate representation of the call spectra was preserved in the AI and MGB at the level present in the IC, while in the case of low-frequency calls (chutter, purr), the representation was less precise in the AI and MGB than in the IC; iii) the difference in the response strength to natural and time-reversed whistle was found to be smaller in the AI than in the IC or MGB.     

Specificity of neuronal responses evoked in the medial geniculate body by stimulation of its different main inputs:In vivo andin vitro investigations

Responses evoked in single neurons of the medial geniculate body (MGB) by electrical stimulation of auditory cortex and fibers of the brachium of the inferior colliculus (BIC) were investigated in vivo and in vitro. In vivo experiments were performed on cats anaesthetized by kalipsol. In vitro experiments were carried out on surviving slices of the rat brain using MGB intranuclear simulation. It has been found that the responses to cortical and nuclear local stimulations show similar peculiarity: an increase in stimulation rate is followed by potentiation and summation of slow EPSPs. At the same time, BIC stimulation evokes mainly fast EPSPs (both in vivo and in vitro) which are remarkably suppressed when rate and intensity of BIC stimulation increase. Distinct features of the MGB neuronal responses to activation of ascending pathways and corticofugal fibers are probably due to differences in anatomical structural among the tested inputs and in chemical mechanisms of the synaptic processes.Neirofiziologiya/Neurophysiology, Vol. 25, No. 3, pp. 203–211, May–June, 1993.     

Unit responses in the cat auditory cortex to medial geniculate body stimulation

Responses of 98 auditory cortical neurons to electrical stimulation of the medial geniculate body (MGB) were recorded (45 extracellulary, 53 intracellularly) in experiments on cats immobilized with tubocurarine. Responses of the same neurons to clicks were recorded for comparison. Of the total number of neurons, 75 (76%) responded both to MGB stimulation and to clicks, and 23 (24%) to MGB stimulation only. The latent period of extracellularly recorded action potentials of auditory cortical neurons in response to clicks varied from 7 to 28 msec (late responses were disregarded), and that to MGB stimulation varied from 1.5 to 12.5 msec. For EPSPs these values were 8–13 and 1–4 msec respectively. The latent period of IPSPs arising in response to MGB stimulation varied from 2.2 to 6.5 msec; for 34% of neurons it did not exceed 3 msec. The difference between the latent periods of responses to clicks and to MGB stimulation varied for different neurons from 6 to 21 msec. Responses of 11% of neurons to MGB stimulation, recorded intracellularly, consisted of sub-threshold EPSPs, while responses of 23% of neurons began with an EPSP which was either followed by an action potential and subsequent IPSP or was at once cut off by an IPSP; 66% of neurons responded with primary IPSPs. Neurons responding to MGB stimulation by primary IPSPs are distributed irregularly in the depth of the cortex: there are very few in layers III and IV and many more at a depth of 1.6–2 mm. Conversely, excited neurons are predominant in layer III and IV, and they are few in number at a depth of 1.6–2 mm. It is concluded that the afferent volley reaching the auditory cortex induces excitation of some neurons therein and, at the same time, by the principle of reciprocity, induces inhibition of others. This afferent inhibition takes place with the participation of inhibitory interneurons, and in some cells the inhibition is recurrent. The existence of reciprocal relationships between neurons in different layers of the auditory cortex is postulated.A. A. Bogomolets' Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 1, pp. 23–31, January–February, 1972.     

Altered Neuronal Intrinsic Properties and Reduced Synaptic Transmission of the Rat's Medial Geniculate Body in Salicylate-Induced Tinnitus

Sodium salicylate (NaSal), an aspirin metabolite, can cause tinnitus in animals and human subjects. To explore neural mechanisms underlying salicylate-induced tinnitus, we examined effects of NaSal on neural activities of the medial geniculate body (MGB), an auditory thalamic nucleus that provides the primary and immediate inputs to the auditory cortex, by using the whole-cell patch-clamp recording technique in MGB slices. Rats treated with NaSal (350 mg/kg) showed tinnitus-like behavior as revealed by the gap prepulse inhibition of acoustic startle (GPIAS) paradigm. NaSal (1.4 mM) decreased the membrane input resistance, hyperpolarized the resting membrane potential, suppressed current-evoked firing, changed the action potential, and depressed rebound depolarization in MGB neurons. NaSal also reduced the excitatory and inhibitory postsynaptic response in the MGB evoked by stimulating the brachium of the inferior colliculus. Our results demonstrate that NaSal alters neuronal intrinsic properties and reduces the synaptic transmission of the MGB, which may cause abnormal thalamic outputs to the auditory cortex and contribute to NaSal-induced tinnitus.     

Processing of Communication Calls in Guinea Pig Auditory Cortex

Vocal communication is an important aspect of guinea pig behaviour and a large contributor to their acoustic environment. We postulated that some cortical areas have distinctive roles in processing conspecific calls. In order to test this hypothesis we presented exemplars from all ten of their main adult vocalizations to urethane anesthetised animals while recording from each of the eight areas of the auditory cortex. We demonstrate that the primary area (AI) and three adjacent auditory belt areas contain many units that give isomorphic responses to vocalizations. These are the ventrorostral belt (VRB), the transitional belt area (T) that is ventral to AI and the small area (area S) that is rostral to AI. Area VRB has a denser representation of cells that are better at discriminating among calls by using either a rate code or a temporal code than any other area. Furthermore, 10% of VRB cells responded to communication calls but did not respond to stimuli such as clicks, broadband noise or pure tones. Area S has a sparse distribution of call responsive cells that showed excellent temporal locking, 31% of which selectively responded to a single call. AI responded well to all vocalizations and was much more responsive to vocalizations than the adjacent dorsocaudal core area. Areas VRB, AI and S contained units with the highest levels of mutual information about call stimuli. Area T also responded well to some calls but seems to be specialized for low sound levels. The two dorsal belt areas are comparatively unresponsive to vocalizations and contain little information about the calls. AI projects to areas S, VRB and T, so there may be both rostral and ventral pathways for processing vocalizations in the guinea pig.     

Temporal Sequence of Visuo-Auditory Interaction in Multiple Areas of the Guinea Pig Visual Cortex

Recent studies in humans and monkeys have reported that acoustic stimulation influences visual responses in the primary visual cortex (V1). Such influences can be generated in V1, either by direct auditory projections or by feedback projections from extrastriate cortices. To test these hypotheses, cortical activities were recorded using optical imaging at a high spatiotemporal resolution from multiple areas of the guinea pig visual cortex, to visual and/or acoustic stimulations. Visuo-auditory interactions were evaluated according to differences between responses evoked by combined auditory and visual stimulation, and the sum of responses evoked by separate visual and auditory stimulations. Simultaneous presentation of visual and acoustic stimulations resulted in significant interactions in V1, which occurred earlier than in other visual areas. When acoustic stimulation preceded visual stimulation, significant visuo-auditory interactions were detected only in V1. These results suggest that V1 is a cortical origin of visuo-auditory interaction.     

Basal forebrain cholinergic input is not essential for lesion-induced plasticity in mature auditory cortex

The putative role of the basal forebrain cholinergic system in mediating lesion-induced plasticity in topographic cortical representations was investigated. Cholinergic immunolesions were combined with unilateral restricted cochlear lesions in adult cats, demonstrating the consequence of cholinergic depletion on lesion-induced plasticity in primary auditory cortex (AI). Immunolesions almost eliminated the cholinergic input to AI, while cochlear lesions produced broad high-frequency hearing losses. The results demonstrate that the near elimination of cholinergic input does not disrupt reorganization of the tonotopic representation of the lesioned (contralateral) cochlea in AI and does not affect the normal representation of the unlesioned (ipsilateral) cochlea. It is concluded that cholinergic basal forebrain input to AI is not essential for the occurrence of lesion-induced plasticity in AI.     

Electrophysiological investigation of conduction of afferent impulses through the medial geniculate body

Extra- and intracellular reactions of 280 neurons of the pars principalis of the medial geniculate body (MGB) and of 408 auditory cortical neurons in area AI to stimulation of the inferior brachium of the midbrain and geniculocortical fibers were studied in cats immobilized with D-tubocurarine. Single electrical stimulation of the inferior brachium was shown to evoke a long and complex neuronal response in MGB in the form of excitation of some and inhibition of other neurons. The initial component of this response lasted 13 msec. Excitation of 72% of neurons participating in the response took place during the first 3 msec after the beginning of stimulation. In the same period 84% of IPSP arose. The inferior brachium was shown to contain a certain number of descending fibers. Some of them are axons of MGB neurons. Many fibers of the inferior brachium reach the auditory cortex without synaptic relay in MGB. Of all cells of MGB excited by stimulation of the inferior brachium monosynaptically, 76% are thalamocortical relay neurons; the rest are interneurons. Of the relay neurons of MGB 90% are excited monosynaptically, the rest by impulses passing through two or three synaptic relays in MGB. During stimulation of the inferior brachium, responses consisting of EPSP-IPSP and primary IPSP are recorded in many neurons of MGB. About 20% of primary IPSP arise monosynaptically, evidently in response to stimulation of inhibitory fibers of the inferior brachium. Most IPSP arise disynaptically, with the participation of an inhibitory interneuron located at the entrance to MGB. Inhibition observed in this case is direct afferent in nature.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 11, No. 6, pp. 515–523, November–December, 1979.     

Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Merionesunguiculatus ): two different coding strategies for pitch and rhythm?

Periodic envelope or amplitude modulations (AM) with periodicities up to several thousand Hertz are characteristic for many natural sounds. Throughout the auditory pathway, signal periodicity is evident in neuronal discharges phase-locked to the envelope. In contrast to lower levels of the auditory pathway, cortical neurons do not phase-lock to periodicities above about 100 Hz. Therefore, we investigated alternative coding strategies for high envelope periodicities at the cortical level. Neuronal responses in the primary auditory cortex (AI) of gerbils to tones and AM were analysed. Two groups of stimuli were tested: (1) AM with a carrier frequency set to the unit's best frequency evoked phase-locked responses which were confined to low modulation frequencies (fms) up to about 100 Hz, and (2) AM with a spectrum completely outside the unit's frequency-response range evoked completely different responses that never showed phase-locking but a rate-tuning to high fms (50 to about 3000 Hz). In contrast to the phase-locked responses, the best fms determined from these latter responses appeared to be topographically distributed, reflecting a periodotopic organization in the AI. Implications of these results for the cortical representation of the perceptual qualities rhythm, roughness and pitch are discussed. Accepted: 25 July 1997     

小鼠初级听皮质神经元的强度调谐特性与机制分析

强度是声音的基本参数之一,听神经元的强度调谐在听觉信息处理方面具有重要意义．以往研究发现γ-氨基丁酸(γ-aminobutyric acid, GABA)能抑制性输入在强度调谐的形成过程中起重要作用,但对抑制性输入与局部神经回路之间的关系并不清楚．本实验通过在体细胞外电生理记录和神经药理学方法,分析了小鼠初级听皮质神经元的强度调谐特性,结果显示：单调型神经元在声刺激强度自中等强度增高时潜伏期缩短(P < 0.05)且发放持续时间延长(P < 0.05),非单调型神经元在声刺激强度自最佳强度增高时潜伏期不变且发放持续时间缩短(P < 0.01)．注射GABA能阻断剂荷包牡丹碱(bicuculline, Bic)后,39.3%的神经元强度调谐类型不变,42.9%的神经元非单调性减弱,17.9%的神经元非单调性增强．表明GABA能抑制并非是形成非单调性的唯一因素,兴奋性输入本身的非单调性和高阈值非GABA能抑制的激活也可能在其中发挥作用．推测由兴奋性和抑制性输入所构成的局部神经功能回路及其整合决定了听皮质神经元的强度调谐特性．     

Learning-induced plasticity in animal and human auditory cortex

Recent data on learning-related changes in animal and human auditory cortex indicate functions beyond mere stimulus representation and simple recognition memory for stimuli. Rather, auditory cortex seems to process and represent stimuli in a task-dependent fashion. This implies plasticity in neural processing, which can be observed at the level of single neuron firing and the level of spatiotemporal activity patterns in cortical areas. Auditory cortex is a structure in which behaviorally relevant aspects of stimulus processing are highly developed because of the fugitive nature of auditory stimuli.     

Auditory Stimuli Mimicking Ambient Sounds Drive Temporal “Delta-Brushes” in Premature Infants

In the premature infant, somatosensory and visual stimuli trigger an immature electroencephalographic (EEG) pattern, “delta-brushes,” in the corresponding sensory cortical areas. Whether auditory stimuli evoke delta-brushes in the premature auditory cortex has not been reported. Here, responses to auditory stimuli were studied in 46 premature infants without neurologic risk aged 31 to 38 postmenstrual weeks (PMW) during routine EEG recording. Stimuli consisted of either low-volume technogenic “clicks” near the background noise level of the neonatal care unit, or a human voice at conversational sound level. Stimuli were administrated pseudo-randomly during quiet and active sleep. In another protocol, the cortical response to a composite stimulus (“click” and voice) was manually triggered during EEG hypoactive periods of quiet sleep. Cortical responses were analyzed by event detection, power frequency analysis and stimulus locked averaging. Before 34 PMW, both voice and “click” stimuli evoked cortical responses with similar frequency-power topographic characteristics, namely a temporal negative slow-wave and rapid oscillations similar to spontaneous delta-brushes. Responses to composite stimuli also showed a maximal frequency-power increase in temporal areas before 35 PMW. From 34 PMW the topography of responses in quiet sleep was different for “click” and voice stimuli: responses to “clicks” became diffuse but responses to voice remained limited to temporal areas. After the age of 35 PMW auditory evoked delta-brushes progressively disappeared and were replaced by a low amplitude response in the same location. Our data show that auditory stimuli mimicking ambient sounds efficiently evoke delta-brushes in temporal areas in the premature infant before 35 PMW. Along with findings in other sensory modalities (visual and somatosensory), these findings suggest that sensory driven delta-brushes represent a ubiquitous feature of the human sensory cortex during fetal stages and provide a potential test of functional cortical maturation during fetal development.     

Reduction of information redundancy in the ascending auditory pathway

Information processing by a sensory system is reflected in the changes in stimulus representation along its successive processing stages. We measured information content and stimulus-induced redundancy in the neural responses to a set of natural sounds in three successive stations of the auditory pathway-inferior colliculus (IC), auditory thalamus (MGB), and primary auditory cortex (A1). Information about stimulus identity was somewhat reduced in single A1 and MGB neurons relative to single IC neurons, when information is measured using spike counts, latency, or temporal spiking patterns. However, most of this difference was due to differences in firing rates. On the other hand, IC neurons were substantially more redundant than A1 and MGB neurons. IC redundancy was largely related to frequency selectivity. Redundancy reduction may be a generic organization principle of neural systems, allowing for easier readout of the identity of complex stimuli in A1 relative to IC.     

Distributed representation of perceptual categories in the auditory cortex

Categorical perception is a process by which a continuous stimulus space is partitioned to represent discrete sensory events. Early experience has been shown to shape categorical perception and enlarge cortical representations of experienced stimuli in the sensory cortex. The present study examines the hypothesis that enlargement in cortical stimulus representations is a mechanism of categorical perception. Perceptual discrimination and identification behaviors were analyzed in model auditory cortices that incorporated sound exposure-induced plasticity effects. The model auditory cortex with over-representations of specific stimuli exhibited categorical perception behaviors for those specific stimuli. These results indicate that enlarged stimulus representations in the sensory cortex may be a mechanism for categorical perceptual learning.     

Human auditory cortical activation during self-vocalization

During speaking, auditory feedback is used to adjust vocalizations. The brain systems mediating this integrative ability have been investigated using a wide range of experimental strategies. In this report we examined how vocalization alters speech-sound processing within auditory cortex by directly recording evoked responses to vocalizations and playback stimuli using intracranial electrodes implanted in neurosurgery patients. Several new findings resulted from these high-resolution invasive recordings in human subjects. Suppressive effects of vocalization were found to occur only within circumscribed areas of auditory cortex. In addition, at a smaller number of sites, the opposite pattern was seen; cortical responses were enhanced during vocalization. This increase in activity was reflected in high gamma power changes, but was not evident in the averaged evoked potential waveforms. These new findings support forward models for vocal control in which efference copies of premotor cortex activity modulate sub-regions of auditory cortex.     

Responses of the neurons of the cortical secondary auditory area to acoustic and non-acoustic stimuli in cats

The responses of the cortical secondary auditory area (AII) to the non-acoustic stimuli (electrical stimulation of the skin in the vibrissae area and light flash) and their combination with acoustic stimulation (sound click or tone) were studied in experiments on cats anesthetized by kalipsol using extra- and intracellular recording. Of the total number of neurons, 69% of the units generating spike responses to the acoustic stimulation responded to the non-acoustic stimulation too. The responses to the modal-nonspecific stimulation, as a rule, were weak and variable; they were mostly represented by a tonic change in the neuronal discharge frequency. The nonspecific stimulation evoked primary excitatory and inhibitory postsynaptic potentials in 77% and 20% of the examined neurons, respectively. We found that synaptic effects of the nonspecific and specific stimulations interact with each other, ensuring considerable modulation of the latter (mostly a significant facilitation resulting from the EPSP summation and suppression of an inhibitory component of the response to acoustic stimulation). Possible participation of the midbrain reticular formation in the transmission of the modal-nonspecific influences to the cortical neurons is considered; stimulation of this structure evoked responses similar to those evoked by the modal-nonspecific sensory stimuli.Neirofiziologiya/Neurophhysiology, Vol. 26, No. 5, pp. 356–364, September–October, 1994.     

Optical imaging of plastic changes induced by fear conditioning in the auditory cortex

The plastic changes in the auditory cortex induced by a fear conditioning, through pairing a sound (CS) with an electric foot-shock (US), were investigated using an optical recording method with voltage sensitive dye, RH795. In order to investigate the effects of association learning, optical signals in the auditory cortex in response to CS (12 kHz pure tone) and non-CS (4, 8, 16 kHz pure tone) were recorded before and after normal and sham conditioning. As a result, the response area to CS enlarged only in the conditioning group after the conditioning. Additionally, the rise time constant of the auditory response to CS significantly decreased and the relative peak value and the decay time constant of the auditory response to CS significantly increased after the conditioning. This study introduces an optical approach to the investigation of fear conditioning, representational plasticity, and the cholinergic system. The findings are synthesized in a model of the synaptic mechanisms that underlie cortical plasticity.     

Columnar Connectivity and Laminar Processing in Cat Primary Auditory Cortex

Background

Radial intra- and interlaminar connections form a basic microcircuit in primary auditory cortex (AI) that extracts acoustic information and distributes it to cortical and subcortical networks. Though the structure of this microcircuit is known, we do not know how the functional connectivity between layers relates to laminar processing.

Methodology/Principal Findings

We studied the relationships between functional connectivity and receptive field properties in this columnar microcircuit by simultaneously recording from single neurons in cat AI in response to broadband dynamic moving ripple stimuli. We used spectrotemporal receptive fields (STRFs) to estimate the relationship between receptive field parameters and the functional connectivity between pairs of neurons. Interlaminar connectivity obtained through cross-covariance analysis reflected a consistent pattern of information flow from thalamic input layers to cortical output layers. Connection strength and STRF similarity were greatest for intralaminar neuron pairs and in supragranular layers and weaker for interlaminar projections. Interlaminar connection strength co-varied with several STRF parameters: feature selectivity, phase locking to the stimulus envelope, best temporal modulation frequency, and best spectral modulation frequency. Connectivity properties and receptive field relationships differed for vertical and horizontal connections.

Conclusions/Significance

Thus, the mode of local processing in supragranular layers differs from that in infragranular layers. Therefore, specific connectivity patterns in the auditory cortex shape the flow of information and constrain how spectrotemporal processing transformations progress in the canonical columnar auditory microcircuit.