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Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex.

Nucleus basalis (NB) neurons are a primary source of neocortical acetylcholine (ACh) and likely contribute to mechanisms of neocortical activation. However, the functions of neocortical activation and its cholinergic component remain unclear. To identify functional consequences of NB activity, we have studied the effects of NB stimulation on thalamocortical transmission. Here we report that tetanic NB stimulation facilitated field potentials, single neuron discharges, and monosynaptic excitatory postsynaptic potentials (EPSPs) elicited in middle to deep cortical layers of the rat auditory cortex following stimulation of the auditory thalamus (medial geniculate, MG). NB stimulation produced a twofold increase in the slope and amplitude of the evoked short-latency (onset 3.0 +/- 0.13 ms, peak 6.3 +/- 0.21 ms), negative-polarity cortical field potential and increased the probability and synchrony of MG-evoked unit discharge, without altering the preceding fiber volley. Intracortical application of atropine blocked the NB-mediated facilitation of field potentials, indicating action of ACh at cortical muscarinic receptors. Intracellular recordings revealed that the short-latency cortical field potential coincided with a short-latency EPSP (onset 3.3 +/- 0.20 ms, peak 5.6 +/- 0.47 ms). NB stimulation decreased the onset and peak latencies of the EPSP by about 20% and increased its amplitude by 26%. NB stimulation also produced slow membrane depolarization and sometimes reduced a long-lasting IPSP that followed the EPSP. The combined effects of NB stimulation served to increase cortical excitability and facilitate the ability of the EPSP to elicit action potentials. Taken together, these data indicate that NB cholinergic neurons can modify neocortical functions by facilitating thalamocortical synaptic transmission.

Animals↗

Tonotopic organization of responses reflecting stop consonant place of articulation in primary auditory cortex (A1) of the monkey.

Current source density and multiunit activity elicited by stop consonant-vowel syllables were examined in primary auditory cortex of an awake monkey. Relative amplitudes of the speech-evoked responses were determined by the onset spectra of the consonants and the tonotopic organization. This finding supports the psychoacoustic hypothesis that the onset spectra of stop consonants are important determinants for the discrimination of place of articulation.

Animals↗

Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex.

Frequency receptive fields (RFs) were determined before and after pairing iontophoretic administration of acetylcholine (ACh) with a repeated single-frequency stimulus in the auditory cortex of barbiturate-anesthetized cats. In 58% of the cells, the paired ACh + tone treatment produced subsequent alterations of frequency RFs. In half of these cases, the RF modifications were highly specific to the frequency that had been paired with ACh. Atropine antagonized the frequency-specific effects of ACh, suggesting that they were mediated via muscarinic cholinergic receptors.

Acetylcholine↗

Tonotopic organization of the auditory cortex: pitch versus frequency representation.

According to the place principles of the classical hearing theory, the physical entity frequency is encoded in the auditory periphery as place information (tonotopic representation), which is decoded in more central parts of the auditory system to form the subjective entity pitch. However, this relation is true only for pure-tone signals (spectral pitch); it can be quite different in the case of complex auditory stimuli (virtual pitch), thus requiring a multistage process for pitch formation. Neuromagnetic measurements showed that the tonotopic organization of the primary auditory cortex reflects the pitch rather than the frequency of the stimulus; that is, the pitch formation process must take place in subcortical regions.

Acoustic Stimulation↗

Development, morphology and topography of chandelier cells in the auditory cortex of the cat.

Using the Golgi method we have studied the development, morphology and topographic distribution of chandelier cells in the auditory cortex of the cat. Kittens from 9 to 42 days old were used. Chandelier cells can be recognized in 9-day-old kittens as a distinct neuronal variety. In the 15- and 23-day-old kittens chandelier cells develop axonal complexes elongated vertically. In the 42-day-old kitten, they seem to have attained their adult morphology. They are not distributed uniformly and their predominance in certain areas suggest that they may have a relation with callosal projecting pyramidal cells.

Animals↗

Development of spectral and temporal response selectivity in the auditory cortex.

The mechanisms by which hearing selectivity is elaborated and refined in early development are very incompletely determined. In this study, we documented contributions of progressively maturing inhibitory influences on the refinement of spectral and temporal response properties in the primary auditory cortex. Inhibitory receptive fields (IRFs) of infant rat auditory cortical neurons were spectrally far broader and had extended over far longer duration than did those of adults. The selective refinement of IRFs was delayed relative to that of excitatory receptive fields by an approximately 2-week period that corresponded to the critical period for plasticity. Local application of a GABA(A) receptor antagonist revealed that intracortical inhibition contributes to this progressive receptive field maturation for response selectivity in frequency. Conversely, it had no effect on the duration of IRFs or successive-signal cortical response recovery times. The importance of exposure to patterned acoustic inputs was suggested when both spectral and temporal IRF maturation were disrupted in rat pups reared in continuous, moderate-intensity noise. They were subsequently renormalized when animals were returned to standard housing conditions as adults.

Animals↗

Functional topography of cat primary auditory cortex: representation of tone intensity.

The neuronal response to tones as a function of intensity was topographically studied with multiple-unit recordings in the primary auditory cortex (AI) of barbiturate-anesthetized cats. The spatial distribution of the characteristics of rate/level functions was determined in each of three intensely studied cases and their relationship to the distribution of spectral parameters (sharpness of tuning and responses to broadband transients) in the same animals was determined. The growth of the high-intensity portion of rate/level functions was estimated by linear regression. Locations with monotonically growing high-intensity portions were spatially segregated from locations with nonmonotonic rate/level functions. Two noncontiguous areas with a high degree of nonmonotonicity were observed. One was located at the dorsoventral center of AI, and a second in the dorsal third of AI. The more ventral aggregate of high nonmonotonicity coincided with the region of sharp frequency tuning. The stimulus levels that produced the highest firing rate (strongest response level, SRL) at any sampled location ranged from 10 to 80 dB sound pressure level (SPL). Several spatial aggregates with either high or low SRLs were observed in AI. The region of sharpest tuning was always associated with a region of low SRLs. The response threshold to contralateral tones at the characteristic frequency (CF) ranged from -10 dB SPL to 85 dB SPL with the majority between 0 and 40 dB SPL. The spatial distribution of response thresholds indicated several segregated areas containing clusters with either higher or lower response thresholds. The correlation of response threshold with integrated bandwidth and transient responses was only weak. Low- and high-intensity tones of the same frequency are represented at different locations in AI as judged by the amount of evoked neuronal activity and are largely independent of the frequency organization. The spatial distribution of locations with high monotonicity and low strongest response levels were aligned with the organization of the integrated excitatory bandwidth and covaried with the response strength to broadband stimuli.

Acoustic Stimulation↗

[A study on the effect of stimulation of amygdaloid complex on the electrical response of auditory cortex in rabbits].

Experiments were performed on 40 adult rabbits immobilized with Flaxedil. The effect of stimulation of amygdaloid complex on the click evoked potential of Woolsey's AI, AII and the auditory cortex behind the rhinal sulcus (ACBRS) was examined by single unit analysis. The results showed that stimulation of lateral nucleus and basal nucleus of amygdala could induce either a facilitory or an inhibitory effect on the evoked potential and the unit discharges. The latency of the inhibitory effect was about 10-25ms, and lasted for 20-115ms. A facilitory effect with a latency as short as 2ms was also observed in one animal. The experimental results indicate that the effect of amygdaloid complex stimulation as transmitted through polysynaptic circuit while the facilitatory effect was monosynaptic. The functional significance of the amygdaloid effect was discussed.

Acoustic Stimulation↗

Cytoarchitecture and sound activated responses in the auditory cortex of the big brown bat, Eptesicus fuscus.

Under free field and closed-system stimulation conditions, we studied the frequency threshold curves, auditory spatial sensitivity and binaurality of neurons in the primary auditory cortex (AC) of the big brown bat, Eptesicus fuscus. All 298 recorded AC neurons discharged phasically. They were recorded at depths less than 1,000 microns with response latencies of 7-25 ms, best frequencies (BFs) of 28-97 kHz and minimum thresholds (MTs) of 8-90 dB SPL. They received excitatory inputs from the contralateral ear and either excitatory (EE) or inhibitory (EI) inputs from the ipsilateral ear. These cortical neurons were tonotopically organized along the anteroposterior axis of the AC. High best frequency neurons were located anteriorly and low best frequency neurons posteriorly. They were most sensitive to sounds delivered from a restricted region of the contralateral frontal auditory space (0 degree-50 degrees in azimuth and 2 degrees up, 15 degrees down in elevation). Frontal auditory space representation appears to be systematically arranged according to the tonotopic axis such that the lateral space is represented posteriorly and the middle space anteriorly. Cortical neurons sequentially isolated from an orthogonally penetrated electrode had similar frequency threshold curves, BFs, MTs, points of maximal auditory spatial sensitivity and binaurality. The EE and EI columns are organized concentrically such that the small number of centrally located EE columns were surrounded by an overwhelming number of EI columns. Using Nissl and Golgi stains as well as c-fos immunocytochemistry, we studied the cytoarchitecture, cell types and sound elicited Fos-like immunoreactivity in the primary AC of this bat species. The primary AC of this bat species can be described into molecular (137 microns), external granular (55 microns), external pyramidal (95 microns), internal granular (102 microns), internal pyramidal (191 microns) and multiform (120 microns) layers. The main type of cells distributed among these six layers are the small, medium and large pyramidal cells. Others include the stellate, horizontal, granular, fusiform, basket, and Martinotii cells. When stimulated with 30 kHz and 79 dB SPL sounds under natural conditions, bilaterally and symmetrically distributed Fos-like immunoreactive neurons were observed in about 20% of neurons in each AC. When stimulated under monaurally plugged conditions, 39-48% more of Fos-like immunoreactive neurons were observed in the ipsilateral AC. This finding supports the fact that the primary AC receives auditory inputs mainly from the contralateral ear.

Acoustic Stimulation↗

LTD and LTP induced by transcranial magnetic stimulation in auditory cortex.

Using a system capable of relatively localized and rapidrate transcranial magnetic stimulation (rTMS), evoked trains of complex spikes were studied in rodent auditory cortex. Low rate rTMS from 1 to 10Hz produced a frequency-dependent increase in spike rate. Iterations of rTMS resulted in long-term potentiation (LTP)-like, and more durable long-term depression (LTD)-like changes in evoked spike rate. These observations generate new perspectives for studying mechanisms of learning and memory non-invasively as well as introducing some caveats for use of rTMS in humans.

Animals↗

The effect of early auditory deprivation on the age-dependent expression pattern of NR2B mRNA in rat auditory cortex.

NMDA receptors have been well shown to be involved in neuronal plasticity. In order to understand the role of NR2B subtype NMDA receptors in auditory function development, the present study investigated the effect of early auditory deprivation on the expression of NR2B mRNA in rat auditory cortex (AC) during postnatal development. For normal rats, the NR2B mRNA expression was highest at birth (postnatal day 1 [P1]) and declined rapidly to low level during adulthood. However, during the critical period of rat auditory development (two to three weeks after birth), there was a transient NR2B expression peak on postnatal day 21 (P21). For the auditory-deprived rats, the general declining trend of NR2B mRNA expression from birth to adult was similar to that observed in the normal group, whereas the expression level from P15 to P27 was significantly lower than normal and the transient peak on P21 disappeared. In both groups, the distribution pattern of NR2B mRNA-positive neurons was also examined in various layers and dorsal, medial and ventral subdistricts of AC. There is no significant effect on the spatial expression of the NR2B mRNA in the AC between normal and deprived group. Our results indicated that the early auditory deprivation decreased the expression levels of NR2B mRNA in AC during the critical period of rat auditory development, suggesting that NR2B plays an important role in the developmental plasticity of auditory function in rats.

Age Factors↗

Properties of a population of GABAergic cells in murine auditory cortex weakly excited by thalamic stimulation.

Feedforward inhibition triggered by thalamocortical (TC) afferents sharpens onset responses and shapes receptive fields of pyramidal cells in auditory cortex (ACx). Previous studies focused only on interneurons located in and around layer IV in primary ACx, target of the dense thalamic projections from ventral medial geniculate. We investigated a population of feedforward interneurons located throughout layers I-V and activated by both afferents from primary and nonprimary thalamus using recordings from auditory TC brain slices obtained from mice expressing green fluorescent protein under control of the glutamic acid decarboxylase (GAD65) promoter in a subpopulation of cortical GABAergic cells. We studied the responses of these interneurons and of pyramidal cells in ACx to thalamic stimulation and to hyper- and depolarizing current pulses. Most interneurons exhibited monosynaptic responses to thalamic stimulation, but this excitation was weak and subthreshold. Interneurons had multipolar dendritic morphology with widespread and dense axonal projections extending several hundred micrometers from the soma. In pyramidal cells from layers II-IV, thalamic excitatory postsynaptic potentials were significantly larger than in interneurons and were superthreshold in 40% of cells, but in these cells, there was no evidence of feedforward inhibition. By contrast, feedforward inhibition was observed in 12 of 18 layer V pyramidal cells. Thus feedforward inhibition in supragranular layers of ACx is weak, and these interneurons require coincident excitation to be activated by thalamic inputs.

Animals↗

Evidence for columnar organization in the auditory cortex of the mouse.

Single cortical auditory neurons sequentially isolated within orthogonal electrode penetrations in the mouse were studied using tonal stimulation. They had common functional properties, such as firing pattern, best frequency, minimum threshold, sharpness of frequency tuning and onset latency. The finding suggests that there is columnar organization in the cortex.

Animals↗

Non-awaking basal forebrain stimulation enhances auditory cortex responsiveness during slow-wave sleep.

Unilateral basal forebrain (BF) stimulations were delivered during slow-wave sleep (SWS) while multi-unit recordings were performed bilaterally in the auditory cortex. Ten tone presentations were followed by 10 pairing trials between BF stimulation and tone. Non-awaking BF stimulations facilitated the tone-evoked responses ipsilaterally only. Atropine blocked the facilitation of the ipsilateral evoked responses observed after pairing in wakefulness. Thus, non-awaking cholinergic input can enhance cortical responsiveness during SWS.

Acoustic Stimulation↗

Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty.

Classical conditioning is known to induce frequency-specific receptive field (RF) plasticity in the auditory cortex (ACx). This study determined the effects of discrimination training on RFs at two levels of task difficulty. Single unit and cluster discharges were recorded in the ACx of adult guinea pigs trained in a tone-shock frequency discrimination paradigm (30 intermixed trials each of positive conditioned stimulus [CS+]-shock and negative CS [CS-] alone) with behavioral performance indexed by the cardiac deceleration conditioned response (CR). After training in an easy task in which subjects developed discriminative CRs, they were trained in a difficult task (reduced frequency distance between CS+ and CS-) in which they failed to discriminate. However, frequency-specific RF plasticity developed at both levels of task difficulty. Responses to the frequency of the CS+ were increased, whereas responses to other frequencies, including the CS- and the prepotent best frequency (BF) were reduced. In many cases, tuning was shifted such that the frequency of the CS+ became the new BF. The effects were present or stronger after a 1-hr retention interval. The role of RF plasticity in the ACx is discussed for behavioral performance and information storage.

Animals↗

Recovery cycles of neurons in the inferior colliculus, the pontine nuclei and the auditory cortex of the big brown bat, Eptesicus fuscus.

This study examines the recovery cycles of neurons in the inferior colliculus (IC), the pontine nuclei (PN) and the auditory cortex (AC) of the big brown bat, Eptesicus fuscus, using a pair of identical pulses at different interpulse intervals. Although the recovery cycle varies among neurons, on average, AC neurons have the longest recovery cycle and PN neurons have the shortest one. The recovery cycle of IC neurons is slightly longer than PN neurons. Neurons tend to have longer recovery cycles when determined with long pulse duration than short one. The minimum threshold of these neurons to the second pulse increases with decreasing interpulse interval. The difference in the recovery cycles of these neurons supports previous findings that IC and PN neurons can follow sound pulses at higher rates than AC neurons do.

Acoustic Stimulation↗