Changes in the acoustically evoked activity in the inferior colliculus of the rat after functional ablation of the auditory cortex

The role of the cortico-tectal pathways in the processing of auditory signals was investigated by recording the click-evoked responses and extracellular multiple unit activity in the inferior colliculus (IC) after functional ablation of the auditory cortex (AC) by local intracortical application of a sodium channel blocker, tetrodotoxin (TTX). Click-evoked IC responses (IC-ER) and multiple unit activity in response to tone bursts were recorded with implanted electrodes in the IC of rats lightly anaesthetized with xylazine. Neural activity was recorded before and after the application of TTX into the ipsilateral auditory cortex (AC) through three implanted cannulas in a total dose of 30 ng. The functional status of the AC was monitored by recording click-evoked middle latency responses from a ball electrode implanted on the AC. During inactivation of the AC, IC-ER amplitudes were either increased (48 % of the cases), decreased (32 % of the cases) or not evidently changed (20 % of the cases). Corresponding effects were observed in the firing rate of IC neurons. Functional ablation of the AC also resulted in a significant prolongation of the latencies of individual waves of the IC-ER. However, the discharge pattern of the multiple unit responses, response thresholds and tuning were not altered during AC inactivation. IC neural activity recovered within several hours, and maximally during 2 days. The results reveal principles of the interaction of cortico-tectal pathways with IC neuronal activity.     

电刺激大马蹄蝠听皮层对下丘神经元听觉敏感性的影响

实验在１２只大马蹄蝠上进行。用常规电生理学方法研究了电刺激听皮层对下丘２１２个神经元的听反应的影响,结果表明,有３２个神经元的听反应被抑制,１９个神经元的听反应褐易化。     

Coding of communication calls in the subcortical and cortical structures of the auditory system

The processing of species-specific communication signals in the auditory system represents an important aspect of animal behavior and is crucial for its social interactions, reproduction, and survival. In this article the neuronal mechanisms underlying the processing of communication signals in the higher centers of the auditory system--inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC)--are reviewed, with particular attention to the guinea pig. The selectivity of neuronal responses for individual calls in these auditory centers in the guinea pig is usually low--most neurons respond to calls as well as to artificial sounds; the coding of complex sounds in the central auditory nuclei is apparently based on the representation of temporal and spectral features of acoustical stimuli in neural networks. Neuronal response patterns in the IC reliably match the sound envelope for calls characterized by one or more short impulses, but do not exactly fit the envelope for long calls. Also, the main spectral peaks are represented by neuronal firing rates in the IC. In comparison to the IC, response patterns in the MGB and AC demonstrate a less precise representation of the sound envelope, especially in the case of longer calls. The spectral representation is worse in the case of low-frequency calls, but not in the case of broad-band calls. The emotional content of the call may influence neuronal responses in the auditory pathway, which can be demonstrated by stimulation with time-reversed calls or by measurements performed under different levels of anesthesia. The investigation of the principles of the neural coding of species-specific vocalizations offers some keys for understanding the neural mechanisms underlying human speech perception.     

Evidence for a Glutamatergic Pathway from the Guinea Pig Auditory Cortex to the Inferior Colliculus

Abstract: We attempt to provide evidence that the projection from the guinea pig auditory cortex (AC) to the inferior colliculus (IC) may contain glutamatergic or GABAergic fibers. Seven days after unilateral AC aspiration, histological studies indicated almost complete AC destruction and preterminal degeneration of fibers and terminal fields in the dorsal cortex (DCIC), external cortex (ECIC), and central nucleus (CNIC) of the IC ipsilateral to the ablated AC. Contralaterally, degeneration appeared in the DCIC. AC ablation depressed the electrically evoked Ca²⁺-dependent release of d -[³H]aspartate ( d -[³H]Asp) in the ipsilateral DCIC, ECIC, and CNIC, and d -[³H]Asp uptake in the CNIC. Together with other evidence that the corticocollicular pathway is excitatory, these findings suggest that this projection may contain glufamatergic and/or aspartatergic (Glu/Asp-ergic) fibers. Glutamic acid decarboxylase immunoreactivity was not apparent in presumed pyramidal cells of layer V of the AC retrogradely labeled with biotinylated dextran injected into the ipsilateral IC. Thus, corticocollicular neurons probably do not synthesize GABA and may not be GABAergic. However, AC ablation depressed [¹⁴C]GABA release from the ipsilateral DCIC and ECIC, and [¹⁴C]GABA uptake in the DCIC. These findings are consistent with the atrophy or down-regulation of some subcortical neurons that mediate GABAergic transmission in the IC.     

Sparse codes for speech predict spectrotemporal receptive fields in the inferior colliculus

We have developed a sparse mathematical representation of speech that minimizes the number of active model neurons needed to represent typical speech sounds. The model learns several well-known acoustic features of speech such as harmonic stacks, formants, onsets and terminations, but we also find more exotic structures in the spectrogram representation of sound such as localized checkerboard patterns and frequency-modulated excitatory subregions flanked by suppressive sidebands. Moreover, several of these novel features resemble neuronal receptive fields reported in the Inferior Colliculus (IC), as well as auditory thalamus and cortex, and our model neurons exhibit the same tradeoff in spectrotemporal resolution as has been observed in IC. To our knowledge, this is the first demonstration that receptive fields of neurons in the ascending mammalian auditory pathway beyond the auditory nerve can be predicted based on coding principles and the statistical properties of recorded sounds.     

Auditory modulation of the inferior temporal cortex neurons in rhesus monkey

We performed a systematic study to check whether neurons in the area TE (the anterior part of inferotemporal cortex) in rhesus monkey, regarded as the last stage of the ventral visual pathway, could be modulated by auditory stimuli. Two fixating rhesus monkeys were presented with visual, auditory or combined audiovisual stimuli while neuronal responses were recorded. We have found that the visually sensitive neurons are also modulated by audiovisual stimuli. This modulation is manifested as the change of response rate. Our results have shown also that the visual neurons were responsive to the sole auditory stimuli. Therefore, the concept of inferotemporal cortex unimodality in information processing should be re-evaluated.     

Chemical stimulation of the thalamic reticular nucleus inhibits the neuronal activity of the posterior insular cortex in rats

Extracellular neuronal responses were recorded from the posterior insular cortex following electrical and chemical stimulation of the thalamic reticular nucleus (Rt) regions. In the present study, most neurons (29/32) were first characterized for their responses to electrical stimulation of the superior laryngeal (SL) nerve or glossopharyngeal (IXth) nerve. In the first experiment, 15 neurons in the posterior insular cortex were examined for their responses to electrical stimulation of the Rt regions. It was found that effective stimulation sites to evoke action potentials in the posterior insular cortex were the ventromedial portion of the Rt and its adjacent regions. In the second experiment, 17 neurons in the posterior insular cortex were examined for their responses by pressure injection of glutamate (Glu) into the Rt regions. Of the 17 neurons, 13 were inhibited in the spontaneous discharge rate following injection of Glu into the Rt, and the remaining four were unaffected. Histologically, it was demonstrated that Glu injection sites for the case of inhibition were located near or within the Rt. On the other hand, the injection sites for all four non-responsive neurons were located outside of the Rt. These data suggest that excitation of the Rt (GABAergic neurons) causes depression of the neuronal activity in the thalamic relay nucleus and then this may in turn induce depressed neuronal activity in the posterior insular cortex. The results here indicate that neuronal activity in the posterior insular cortex is controlled by the Rt, which has been reported in other sensory systems.     

Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus

Responses of 117 single- or multi-units in the auditory cortex (AC) of bats (Myotis lucifugus) to tone bursts of different stimulus durations (1– 400 ms) were studied over a wide range of stimulus intensities to determine how stimulus duration is represented in the AC. 36% of AC neurons responded more strongly to short stimulus durations showing short-pass duration response functions, 31% responded equally to all pulse durations (i.e., all-pass), 18% responded preferentially to stimuli having longer durations (i.e., long-pass), and 15% responded to a narrow range of stimulus durations (i.e., band-pass). Neurons showing long-pass and short-pass duration response functions were narrowly distributed within two horizontal slabs of the cortex, over the rostrocaudal extent of the AC. The effects of stimulus level on duration selectivity were evaluated for 17 AC neurons. For 65% of these units, an increase in stimulus intensity resulted in a progressive decrease in the best duration. In light of the unusual intensity-dependent duration responses of AC neurons, we hypothesized that the response selectivities of AC neurons is different from that in the brainstem. This hypothesis was validated by results of study of the duration response characteristics of single neurons in the inferior colliculus. Accepted: 8 November 1996     

GABA-mediated modulation of the discharge pattern and rate-level function of two simultaneously recorded neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus

Neurons in the central nucleus of the inferior colliculus (IC) receive excitatory and inhibitory inputs from both lower and higher auditory nuclei. Interaction of these two opposing inputs shapes response properties of IC neurons. In this study, we examine the interaction of excitation and inhibition on the responses of two simultaneously recorded IC neurons using a probe and a masker under forward masking paradigm. We specifically study whether a sound that serves as a probe to elicit responses of one neuron might serve as a masker to suppress or facilitate the responses of the other neuron. For each pair of IC neurons, we deliver the probe at the best frequency (BF) of one neuron and the masker at the BF of the other neuron and vice versa. Among 33 pairs of IC neurons recorded, this forward masking produces response suppression in 29 pairs of IC neurons and response facilitation in 4 pairs of IC neurons. The degree of suppression decreases with recording depth, sound level and BF difference between each pair of IC neurons. During bicuculline application, the degree of response suppression decreases in the bicuculline-applied neuron but increases in the paired neuron. Our data indicate that the forward masking of responses of IC neurons observed in this study is mostly mediated through GABAergic inhibition which also shapes the discharge pattern of these neurons. These data suggest that interaction among individual IC neurons improves auditory sensitivity during auditory signal processing.     

Distributed coding of sound locations in the auditory cortex

Although the auditory cortex plays an important role in sound localization, that role is not well understood. In this paper, we examine the nature of spatial representation within the auditory cortex, focusing on three questions. First, are sound-source locations encoded by individual sharply tuned neurons or by activity distributed across larger neuronal populations? Second, do temporal features of neural responses carry information about sound-source location? Third, are any fields of the auditory cortex specialized for spatial processing? We present a brief review of recent work relevant to these questions along with the results of our investigations of spatial sensitivity in cat auditory cortex. Together, they strongly suggest that space is represented in a distributed manner, that response timing (notably first-spike latency) is a critical information-bearing feature of cortical responses, and that neurons in various cortical fields differ in both their degree of spatial sensitivity and their manner of spatial coding. The posterior auditory field (PAF), in particular, is well suited for the distributed coding of space and encodes sound-source locations partly by modulations of response latency. Studies of neurons recorded simultaneously from PAF and/or A1 reveal that spatial information can be decoded from the relative spike times of pairs of neurons - particularly when responses are compared between the two fields - thus partially compensating for the absence of an absolute reference to stimulus onset.     

Responses of neurons in the rat auditory and associative cortices to tonal stimuli

Activity of single neurons and mass evoked potentials (EP) were recorded from the auditory (area 41) and associative (area 39) cortices in acute experiments on rats anesthetized with urethane, nembutal, or chloralose; pure tones were used as acoustic stimuli. The EP appearing in response to a wide range of sound tones on the surface of the auditory and associative cortices were dissimilar in their latency and shape. For neurons exhibiting stable responses, the frequency-threshold curves (FTC) were plotted.Weak and variable responses of neurons were observed under slight urethane anesthesia. Nembutal anesthesia increased the responsiveness of neurons and the probability of appearing of late components in the responses. Chloralose anesthesia was characterized by extension of frequency range perceived by a neuron, while its sharpness of tuning remained unchanged. Under all types of anesthesia employed, the responses recorded from the associative cortex neurons had longer latencies than those recorded from the auditory cortex neurons. Neurons exhibiting the frequency selectivity were much less numerous in the associative cortex than in the auditory cortex. The former neurons were often characterized by intermittent FTC and they responded to a more extended frequency range. No clear tonotopic organization was found in the associative cortex.Neirofiziologiya/Neurophysiology, Vol. 25, No. 5, pp. 343–349, September–October, 1993.     

Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex

The mismatch negativity (MMN) is a key biomarker of automatic deviance detection thought to emerge from 2 cortical sources. First, the auditory cortex (AC) encodes spectral regularities and reports frequency-specific deviances. Then, more abstract representations in the prefrontal cortex (PFC) allow to detect contextual changes of potential behavioral relevance. However, the precise location and time asynchronies between neuronal correlates underlying this frontotemporal network remain unclear and elusive. Our study presented auditory oddball paradigms along with “no-repetition” controls to record mismatch responses in neuronal spiking activity and local field potentials at the rat medial PFC. Whereas mismatch responses in the auditory system are mainly induced by stimulus-dependent effects, we found that auditory responsiveness in the PFC was driven by unpredictability, yielding context-dependent, comparatively delayed, more robust and longer-lasting mismatch responses mostly comprised of prediction error signaling activity. This characteristically different composition discarded that mismatch responses in the PFC could be simply inherited or amplified downstream from the auditory system. Conversely, it is more plausible for the PFC to exert top-down influences on the AC, since the PFC exhibited flexible and potent predictive processing, capable of suppressing redundant input more efficiently than the AC. Remarkably, the time course of the mismatch responses we observed in the spiking activity and local field potentials of the AC and the PFC combined coincided with the time course of the large-scale MMN-like signals reported in the rat brain, thereby linking the microscopic, mesoscopic, and macroscopic levels of automatic deviance detection.

Neuronal recordings in the medial prefrontal cortex of the rat demonstrate that auditory mismatch responses are purely composed of prediction error signaling activity, independent from the spectral effects that drive the auditory system.     

M-channels modulate the intrinsic excitability and synaptic responses of layer 2/3 pyramidal neurons in auditory cortex

Neurons in the auditory cortex are believed to utilize temporal patterns of neural activity to accurately process auditory information but the intrinsic neuronal mechanism underlying the control of auditory neural activity is not known. The slowly activating, persistent K⁺ channel, also called M-channel that belongs to the Kv7 family, is already known to be important in regulating subthreshold neural excitability and synaptic summation in neocortical and hippocampal pyramidal neurons. However, its functional role in the primary auditory cortex (A1) has never been characterized. In this study, we investigated the roles of M-channels on neuronal excitability, short-term plasticity, and synaptic summation of A1 layer 2/3 regular spiking pyramidal neurons with whole-cell current-clamp recordings in vitro. We found that blocking M-channels with a selective M-channel blocker, XE991, significantly increased neural excitability of A1 layer 2/3 pyramidal neurons. Furthermore, M-channels controled synaptic responses of intralaminar-evoked excitatory postsynaptic potentials (EPSPs); XE991 significantly increased EPSP amplitude, decreased the rate of short-term depression, and increased the synaptic summation. These results suggest that M-channels are involved in controlling spike output patterns and synaptic responses of A1 layer 2/3 pyramidal neurons, which would have important implications in auditory information processing.     

不同时程弱前掩蔽声对小鼠下丘神经元声反应的选择性抑制

自由声场条件下,以强度为神经元最小阈值阈上5dB,时程分别为40、60、80和100ms的纯音作为前掩蔽声,观察和记录了不同时程弱前掩蔽声对小鼠（Musmusculus Km）下丘神经元发放和声强处理的影响。实验记录到154个神经元,对其中的104个神经元做了不同时程掩蔽声影响的测试。结果发现：掩蔽声对神经元放电率的抑制作用在时间上表现为前抑制（41％）、后抑制（9％）和全抑制（50％）三种类型。改变掩蔽声时程时,大部分神经元（72％）的抑制类型不发生改变,但少部分神经元（28％）随掩蔽声时程的增加,大量的后抑制类型转变为前抑制或全抑制类型。此外,超过一半的神经元（58．06％）其强度．放电率函数曲线随掩蔽声时程的改变而发生转变,主要表现为单调型向饱和型转变及饱和型向非单调型转变,这种转变并不随掩蔽声时程增加表现出规律性的变化。结果表明,前掩蔽作用于下丘神经元声反应的时间域和强度域时具有不均衡性,推测不同时程弱前掩蔽声激活的抑制性输入能分化性调制下丘神经元声反应特性。     

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     

Expression of Immediate-Early Genes in the Inferior Colliculus and Auditory Cortex in Salicylate-Induced Tinnitus in Rat

Tinnitus could be associated with neuronal hyperactivity in the auditory center. As a neuronal activity marker, immediate-early gene (IEG) expression is considered part of a general neuronal response to natural stimuli. Some IEGs, especially the activity-dependent cytoskeletal protein (Arc) and the early growth response gene-1 (Egr-1), appear to be highly correlated with sensory-evoked neuronal activity. We hypothesize, therefore, an increase of Arc and Egr-1 will be observed in a tinnitus model. In our study, we used the gap prepulse inhibition of acoustic startle (GPIAS) paradigm to confirm that salicylate induces tinnitus-like behavior in rats. However, expression of the Arc gene and Egr-1 gene were decreased in the inferior colliculus (IC) and auditory cortex (AC), in contradiction of our hypothesis. Expression of N-methyl D-aspartate receptor subunit 2B (NR2B) was increased and all of these changes returned to normal 14 days after treatment with salicylate ceased. These data revealed long-time administration of salicylate induced tinnitus markedly but reversibly and caused neural plasticity changes in the IC and the AC. Decreased expression of Arc and Egr-1 might be involved with instability of synaptic plasticity in tinnitus.Key words: salicylate, inferior colliculus, auditory cortex, activity-dependent cytoskeletal protein, early growth response gene-1     

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.     

Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.     

Unit responses in the auditory cortex to stimulation of geniculocortical fibers

Extracellular and intracellular single unit responses of neurons of the auditory cortex to electrical stimulation of geniculocortical fibers (GCF) were recorded in experiments on cats immobilized with tubocurarine. The latent period of responses of 15% of neurons to GCF stimulation was 0.3–1.5 msec. It is postulated that they were excited anti-dromically. The latent period of spikes generated by neurons responding to GCF stimulation orthodromically varied from 1.6 to 12 msec. In 28.6% of neurons the latent period was 1.6–2.5 msec. It is postulated that these neurons were excited monosynaptically. Intracellular recording revealed primary IPSPs in response to GCF stimulation in 63.3% of neurons, a brief EPSP followed by a prolonged IPSP in 17.7%, an EPSP-spike-IPSP complex in 12.3%, and subthreshold EPSPs in 7% of neurons. The latent period of the primary IPSPs varied from 1.8 to 11 msec, being 1.8–3.7 in 72%, 3.8–5.7 in 20.0%, and 5.8–11 msec in 8.0% of neurons. The latent period of responses beginning with an EPSP was 1–4 msec (mean 1.8 msec). Orthodromic responses arising 3–10 msec after the antidromic response, and consisting of 3–5 spikes, were recorded in some antidromically excited neurons. Hypotheses regarding the functional organization of the auditory cortex and mechanisms of inhibition in its neurons are put forward on the basis of the results obtained.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 3, pp. 227–235, May–June, 1972.     

Sparse representation of sounds in the unanesthetized auditory cortex

How do neuronal populations in the auditory cortex represent acoustic stimuli? Although sound-evoked neural responses in the anesthetized auditory cortex are mainly transient, recent experiments in the unanesthetized preparation have emphasized subpopulations with other response properties. To quantify the relative contributions of these different subpopulations in the awake preparation, we have estimated the representation of sounds across the neuronal population using a representative ensemble of stimuli. We used cell-attached recording with a glass electrode, a method for which single-unit isolation does not depend on neuronal activity, to quantify the fraction of neurons engaged by acoustic stimuli (tones, frequency modulated sweeps, white-noise bursts, and natural stimuli) in the primary auditory cortex of awake head-fixed rats. We find that the population response is sparse, with stimuli typically eliciting high firing rates (>20 spikes/second) in less than 5% of neurons at any instant. Some neurons had very low spontaneous firing rates (<0.01 spikes/second). At the other extreme, some neurons had driven rates in excess of 50 spikes/second. Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported. Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex. Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.