scholarly journals Tone-Evoked Excitatory and Inhibitory Synaptic Conductances of Primary Auditory Cortex Neurons

2004 ◽  
Vol 92 (1) ◽  
pp. 630-643 ◽  
Author(s):  
Andrew Y. Y. Tan ◽  
Li I. Zhang ◽  
Michael M. Merzenich ◽  
Christoph E. Schreiner

In primary auditory cortex (AI) neurons, tones typically evoke a brief depolarization, which can lead to spiking, followed by a long-lasting hyperpolarization. The extent to which the hyperpolarization is due to synaptic inhibition has remained unclear. Here we report in vivo whole cell voltage-clamp measurements of tone-evoked excitatory and inhibitory synaptic conductances of AI neurons of the pentobarbital-anesthetized rat. Tones evoke an increase of excitatory synaptic conductance, followed by an increase of inhibitory synaptic conductance. The synaptic conductances can account for the gross time course of the typical membrane potential response. Synaptic excitation and inhibition have the same frequency tuning. As tone intensity increases, the amplitudes of synaptic excitation and inhibition increase, and the latency of synaptic excitation decreases. Our data indicate that the interaction of synaptic excitation and inhibition shapes the time course and frequency tuning of the spike responses of AI neurons.

2018 ◽  
Author(s):  
Huan-huan Zeng ◽  
Jun-feng Huang ◽  
Ming Chen ◽  
Yun-qing Wen ◽  
Zhi-ming Shen ◽  
...  

AbstractMarmoset has emerged as a useful non-human primate species for studying the brain structure and function. Previous studies on the mouse primary auditory cortex (A1) showed that neurons with preferential frequency tuning responses are mixed within local cortical regions, despite a large-scale tonotopic organization. Here we found that frequency tuning properties of marmoset A1 neurons are highly uniform within local cortical regions. We first defined tonotopic map of A1 using intrinsic optical imaging, and then used in vivo two-photon calcium imaging of large neuronal populations to examine the tonotopic preference at the single-cell level. We found that tuning preferences of layer 2/3 neurons were highly homogeneous over hundreds of micrometers in both horizontal and vertical directions. Thus, marmoset A1 neurons are distributed in a tonotopic manner at both macro- and microscopic levels. Such organization is likely to be important for the organization of auditory circuits in the primate brain.


2019 ◽  
Vol 116 (50) ◽  
pp. 25304-25310 ◽  
Author(s):  
Pei-Ann Lin ◽  
Samuel K. Asinof ◽  
Nicholas J. Edwards ◽  
Jeffry S. Isaacson

Changes in arousal influence cortical sensory representations, but the synaptic mechanisms underlying arousal-dependent modulation of cortical processing are unclear. Here, we use 2-photon Ca2+ imaging in the auditory cortex of awake mice to show that heightened arousal, as indexed by pupil diameter, broadens frequency-tuned activity of layer 2/3 (L2/3) pyramidal cells. Sensory representations are less sparse, and the tuning of nearby cells more similar when arousal increases. Despite the reduction in selectivity, frequency discrimination by cell ensembles improves due to a decrease in shared trial-to-trial variability. In vivo whole-cell recordings reveal that mechanisms contributing to the effects of arousal on sensory representations include state-dependent modulation of membrane potential dynamics, spontaneous firing, and tone-evoked synaptic potentials. Surprisingly, changes in short-latency tone-evoked excitatory input cannot explain the effects of arousal on the broadness of frequency-tuned output. However, we show that arousal strongly modulates a slow tone-evoked suppression of recurrent excitation underlying lateral inhibition [H. K. Kato, S. K. Asinof, J. S. Isaacson, Neuron, 95, 412–423, (2017)]. This arousal-dependent “network suppression” gates the duration of tone-evoked responses and regulates the broadness of frequency tuning. Thus, arousal can shape tuning via modulation of indirect changes in recurrent network activity.


2019 ◽  
Vol 116 (8) ◽  
pp. 3239-3244 ◽  
Author(s):  
Huan-huan Zeng ◽  
Jun-feng Huang ◽  
Ming Chen ◽  
Yun-qing Wen ◽  
Zhi-ming Shen ◽  
...  

Marmoset has emerged as a useful nonhuman primate species for studying brain structure and function. Previous studies on the mouse primary auditory cortex (A1) showed that neurons with preferential frequency-tuning responses are mixed within local cortical regions, despite a large-scale tonotopic organization. Here we found that frequency-tuning properties of marmoset A1 neurons are highly uniform within local cortical regions. We first defined the tonotopic map of A1 using intrinsic optical imaging and then used in vivo two-photon calcium imaging of large neuronal populations to examine the tonotopic preference at the single-cell level. We found that tuning preferences of layer 2/3 neurons were highly homogeneous over hundreds of micrometers in both horizontal and vertical directions. Thus, marmoset A1 neurons are distributed in a tonotopic manner at both macro- and microscopic levels. Such organization is likely to be important for the organization of auditory circuits in the primate brain.


2020 ◽  
Author(s):  
Bernard J. Slater ◽  
Jeffry S. Isaacson

AbstractSensory cortical areas receive glutamatergic callosal projections that link information processing between brain hemispheres. However, the role of interhemispheric projections in sensory processing is unclear. Here we use single unit recordings and optogenetic manipulations in awake mice to probe how callosal inputs modulate spontaneous and tone-evoked activity in primary auditory cortex (A1). Although activation of callosal fibers increased firing of some pyramidal cells, the majority of responsive cells were suppressed. In contrast, callosal stimulation consistently increased fast spiking (FS) cell activity and brain slice recordings indicated that parvalbumin (PV)-expressing cells receive stronger callosal input than pyramidal cells or other interneuron subtypes. In vivo silencing of the contralateral cortex revealed that callosal inputs linearly modulate tone-evoked pyramidal cell activity via both multiplicative and subtractive operations. These results suggest that callosal input regulates both the salience and tuning sharpness of tone responses in A1 via PV cell-mediated feedforward inhibition.


2001 ◽  
Vol 85 (6) ◽  
pp. 2350-2358 ◽  
Author(s):  
Sanjiv K. Talwar ◽  
Pawel G. Musial ◽  
George L. Gerstein

Studies in several mammalian species have demonstrated that bilateral ablations of the auditory cortex have little effect on simple sound intensity and frequency-based behaviors. In the rat, for example, early experiments have shown that auditory ablations result in virtually no effect on the rat's ability to either detect tones or discriminate frequencies. Such lesion experiments, however, typically examine an animal's performance some time after recovery from ablation surgery. As such, they demonstrate that the cortex is not essential for simple auditory behaviors in the long run. Our study further explores the role of cortex in basic auditory perception by examining whether the cortex is normally involved in these behaviors. In these experiments we reversibly inactivated the rat primary auditory cortex (AI) using the GABA agonist muscimol, while the animals performed a simple auditory task. At the same time we monitored the rat's auditory activity by recording auditory evoked potentials (AEP) from the cortical surface. In contrast to lesion studies, the rapid time course of these experimental conditions preclude reorganization of the auditory system that might otherwise compensate for the loss of cortical processing. Soon after bilateral muscimol application to their AI region, our rats exhibited an acute and profound inability to detect tones. After a few hours this state was followed by a gradual recovery of normal hearing, first of tone detection and, much later, of the ability to discriminate frequencies. Surface muscimol application, at the same time, drastically altered the normal rat AEP. Some of the normal AEP components vanished nearly instantaneously to unveil an underlying waveform, whose size was related to the severity of accompanying behavioral deficits. These results strongly suggest that the cortex is directly involved in basic acoustic processing. Along with observations from accompanying multiunit experiments that related the AEP to AI neuronal activity, our results suggest that a critical amount of activity in the auditory cortex is necessary for normal hearing. It is likely that the involvement of the cortex in simple auditory perceptions has hitherto not been clearly understood because of underlying recovery processes that, in the long-term, safeguard fundamental auditory abilities after cortical injury.


2021 ◽  
Vol 15 ◽  
Author(s):  
Wenlu Pan ◽  
Jing Pan ◽  
Yan Zhao ◽  
Hongzheng Zhang ◽  
Jie Tang

Serotonin transporter (SERT) modulates the level of 5-HT and significantly affects the activity of serotonergic neurons in the central nervous system. The manipulation of SERT has lasting neurobiological and behavioral consequences, including developmental dysfunction, depression, and anxiety. Auditory disorders have been widely reported as the adverse events of these mental diseases. It is unclear how SERT impacts neuronal connections/interactions and what mechanism(s) may elicit the disruption of normal neural network functions in auditory cortex. In the present study, we report on the neuronal morphology and function of auditory cortex in SERT knockout (KO) mice. We show that the dendritic length of the fourth layer (L-IV) pyramidal neurons and the second-to-third layer (L-II/III) interneurons were reduced in the auditory cortex of the SERT KO mice. The number and density of dendritic spines of these neurons were significantly less than those of wild-type neurons. Also, the frequency-tonotopic organization of primary auditory cortex was disrupted in SERT KO mice. The auditory neurons of SERT KO mice exhibited border frequency tuning with high-intensity thresholds. These findings indicate that SERT plays a key role in development and functional maintenance of auditory cortical neurons. Auditory function should be examined when SERT is selected as a target in the treatment for psychiatric disorders.


1999 ◽  
Vol 82 (5) ◽  
pp. 2327-2345 ◽  
Author(s):  
Jagmeet S. Kanwal ◽  
Douglas C. Fitzpatrick ◽  
Nobuo Suga

Mustached bats, Pteronotus parnellii parnellii,emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF1-4) component followed by a short, frequency-modulated (FM1-4) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF2 is maintained within a narrowband centered at ∼61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63.0-kHz frequencies in the “Doppler-shifted CF processing” (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of ∼25 kHz (BFlow) and ∼61 kHz (BFhigh). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BFlowcorresponding to a frequency in the lower half of the echolocation pulse FM1 sweep and another of sharp tuning to frequencies centered at BFhigh corresponding to the CF2 in the echo. Facilitative response areas for BFhigh are broadened by ∼0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BFhigh response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BFhigh. About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BFhigh so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BFhigh and sometimes for BFlow. Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area.


1998 ◽  
Vol 80 (5) ◽  
pp. 2743-2764 ◽  
Author(s):  
Jos J. Eggermont

Eggermont, Jos J. Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. J. Neurophysiol. 80: 2743–2764, 1998. This study investigates the degree of similarity of three different auditory cortical areas with respect to the coding of periodic stimuli. Simultaneous single- and multiunit recordings in response to periodic stimuli were made from primary auditory cortex (AI), anterior auditory field (AAF), and secondary auditory cortex (AII) in the cat to addresses the following questions: is there, within each cortical area, a difference in the temporal coding of periodic click trains, amplitude-modulated (AM) noise bursts, and AM tone bursts? Is there a difference in this coding between the three cortical fields? Is the coding based on the temporal modulation transfer function (tMTF) and on the all-order interspike-interval (ISI) histogram the same? Is the perceptual distinction between rhythm and roughness for AM stimuli related to a temporal versus spatial representation of AM frequency in auditory cortex? Are interarea differences in temporal response properties related to differences in frequency tuning? The results showed that: 1) AM stimuli produce much higher best modulation frequencies (BMFs) and limiting rates than periodic click trains. 2) For periodic click trains and AM noise, the BMFs and limiting rates were not significantly different for the three areas. However, for AM tones the BMF and limiting rates were about a factor 2 lower in AAF compared with the other areas. 3) The representation of stimulus periodicity in ISIs resulted in significantly lower mean BMFs and limiting rates compared with those estimated from the tMTFs. The difference was relatively small for periodic click trains but quite large for both AM stimuli, especially in AI and AII. 4) Modulation frequencies <20 Hz were represented in the ISIs, suggesting that rhythm is coded in auditory cortex in temporal fashion. 5) In general only a modest interdependence of spectral- and temporal-response properties in AI and AII was found. The BMFs were correlated positively with characteristic frequency in AAF. The limiting rate was positively correlated with the frequency-tuning curve bandwidth in AI and AII but not in AAF. Only in AAF was a correlation between BMF and minimum latency was found. Thus whereas differences were found in the frequency-tuning curve bandwidth and minimum response latencies among the three areas, the coding of periodic stimuli in these areas was fairly similar with the exception of the very poor representation of AM tones in AII. This suggests a strong parallel processing organization in auditory cortex.


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