Ultrastructural organization of efferent fiber endings in zones A1 and A4 of the cat auditory cortex in the superior olivary complex.
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In order to find the cortical neural activities that reflect musical processing, we conducted measurements of MEG responses while subjects listened to familiar melodies. Significant enlargement of the N1m peak was observed in the response to the endnote of a phrase that was deviated to out-of-key from the keynote. Equivalent current sources of the enlarged N1m response were localized in the cortical area of the superior temporal plane. These results suggest the possibility of fast neural processing, as early as 100 ms, of the auditory cortex detecting incongruity of a melody.
The inhibitory neurotransmitter gamma-aminobutyric acid (GABA) is thought to play an important role in activity-dependent stages of brain development. Previous studies have shown that different functional subclasses of cortical GABA-containing neurons can be distinguished by antibodies to the calcium-binding proteins parvalbumin and calbindin. Thus insight into the development of distinct subsets of inhibitory cortical circuits can be gained by studying the development of these calcium-binding protein-containing neurons. Previous studies in several mammalian species have suggested that calcium-binding proteins are upregulated in sensory cortex when thalamocortical afferents arrive. In ferrets, the ingrowth of thalamic axons into cortex occurs well into postnatal development, allowing access to early stages of cortical development and calcium-binding protein expression. We find in ferrets that both parvalbumin- and calbindin-immunoreactivity are present in primary visual and primary auditory cortex long before thalamocortical synapse formation, but that there is a sharp decline in immunoreactivity by postnatal day 20. Day 20 in ferrets corresponds to postnatal day 1 in cats, and thus previous studies in postnatal cats would have missed this early pattern of calcium-binding protein distribution. Another surprising finding is that the proportion of parvalbumin- and calbindin-immunoreactive neurons peaks secondarily late in development, between P60 and adulthood. This result suggests that the parvalbumin- and calbindin-containing subclasses of nonpyramidal neurons remain immature until late in the critical period for cortical plasticity, and that they are positioned to play an important role in experience-dependent modification of cortical circuits.
Cortical responses are adjusted and optimized throughout life to meet changing behavioral demands and to compensate for peripheral damage. The cholinergic nucleus basalis (NB) gates cortical plasticity and focuses learning on behaviorally meaningful stimuli. By systematically varying the acoustic parameters of the sound paired with NB activation, we have previously shown that tone frequency and amplitude modulation rate alter the topography and selectivity of frequency tuning in primary auditory cortex. This result suggests that network-level rules operate in the cortex to guide reorganization based on specific features of the sensory input associated with NB activity. This report summarizes recent evidence that temporal response properties of cortical neurons are influenced by the spectral characteristics of sounds associated with cholinergic modulation. For example, repeated pairing of a spectrally complex (ripple) stimulus decreased the minimum response latency for the ripple, but lengthened the minimum latency for tones. Pairing a rapid train of tones with NB activation only increased the maximum following rate of cortical neurons when the carrier frequency of each train was randomly varied. These results suggest that spectral and temporal parameters of acoustic experiences interact to shape spectrotemporal selectivity in the cortex. Additional experiments with more complex stimuli are needed to clarify how the cortex learns natural sounds such as speech.
The oscine song system, a set of interconnected brain nuclei involved in song production and learning, is one of the first and clearest examples of brain sexual dimorphism in a vertebrate, being typically well-developed in males, but not females. Here we present evidence for a sexual dimorphism in the caudomedial nidopallidum (NCM), an auditory area outside of the song system. NCM is thought to correspond to a portion of the auditory cortex of mammals and is involved in the perceptual processing of birdsong. We show that cells immunolabeled for the calcium-binding protein calbindin are primarily localized to caudal NCM and are almost twice as numerous in males as in females. We demonstrate that calbindin-positive cells constitute a subset of GABAergic cells in NCM, and show that the sex dimorphism in this cell population does not result from local gender differences in the overall density of neuronal or GABAergic cells. In addition, we demonstrate that calbindin-positive cells lack song-induced expression of the activity-dependent gene ZENK, and that song stimulation does not change the density or distribution of these cells in NCM. Finally, we show that the distribution of calbindin-positive cells in NCM is strikingly similar to the mRNA expression for the estrogen-generating enzyme aromatase. Together these results suggest that NCM is likely composed of neurochemically-distinct domains and presents a marked sex dimorphism in a specific subset of GABAergic neurons, which may confer sex-specific sensory processing capabilities to this auditory area. Our results also suggest that local sex steroid hormones may play a local role in auditory processing in the songbird telencephalon.
Physiological and immunocytochemical evidence indicates a layer-dependent organization of inhibitory circuits in the neocortex. To investigate the contribution of GABAergic inhibition to frequency tuning in the different cortical layers, we recorded single and multiple units in near-radial penetrations before and during iontophoretic application of the GABA(A)-receptor antagonist bicuculline in the auditory cortex of the lightly anesthetized gerbil. Bicuculline generally increased the spontaneous rate and enhanced and prolonged onset activity. Application of bicuculline often resulted in a shift of best frequency and a decrease of threshold (5.5 dB). A broadening of the frequency tuning evident by lower Q40dB values was observed in 63% of the units. In units with multipeaked tuning curves or clearly separated response areas, bicuculline application removed the inhibitory regions and created single-peaked tuning curves. The influence of bicuculline on the receptive field size was not significantly layer-specific but tended to be most pronounced in layers V and VI. In layer VI, we frequently found "silent" neurons that responded to sound only when GABAergic inhibition was antagonized. From the analysis of postembedding GABA immunocytochemistry, the proportion of GABAergic neurons was found to be maximal in layers I and V, and the number of GABAergic perisomatic puncta (axon terminals) on cell somata peaked in layer V.
Correlation-based synaptic plasticity provides a potential cellular mechanism for learning and memory. Studies in the visual and somatosensory systems have shown that behavioral and surgical manipulation of sensory inputs leads to changes in cortical organization that are consistent with the operation of these learning rules. In this study, we examine how the organization of primary auditory cortex (A1) is altered by tones designed to decrease the average input correlation across the frequency map. After one month of separately pairing nucleus basalis stimulation with 2 and 14 kHz tones, a greater proportion of A1 neurons responded to frequencies below 2 kHz and above 14 kHz. Despite the expanded representation of these tones, cortical excitability was specifically reduced in the high and low frequency regions of A1, as evidenced by increased neural thresholds and decreased response strength. In contrast, in the frequency region between the two paired tones, driven rates were unaffected and spontaneous firing rate was increased. Neural response latencies were increased across the frequency map when nucleus basalis stimulation was associated with asynchronous activation of the high and low frequency regions of A1. This set of changes did not occur when pulsed noise bursts were paired with nucleus basalis stimulation. These results are consistent with earlier observations that sensory input statistics can shape cortical map organization and spike timing.
Neuromagnetic responses were recorded to 33-ms frequency-glide tones with a 7-channel SQUID gradiometer. Ninety per cent of the tones were of rising/falling frequency and 10% otherwise similar tones but presented backwards, i.e. comparable falling/rising frequency glides. The infrequent stimuli elicited a specific response, the mismatch field (MMF), whose equivalent source suggested a generation in the supratemporal auditory cortex. Responses to rising and falling infrequent glides showed no consistent asymmetry. The MMF amplitude correlated positively with the glide magnitude. It is suggested that the generation of MMF to changes in the direction of frequency glides involves neuronal networks tuned to frequency glides.