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Interaction of excitatory and inhibitory frequency-receptive fields in determining fundamental frequency sensitivity of primary auditory cortex neurons in awake cats.

Harmonic complex tones produce pitch-height perception corresponding to the fundamental frequency (F0). This study investigates how the spectral cue of F0 is processed in neurons of the primary auditory cortex (A1) with sustained-response properties. We found F0-sensitive and -insensitive cells: the former discriminated between harmonics and noise, while the latter did not. F0-sensitive cells preferred F0s corresponding to the best frequency (BF) and 0.5 x BF. The F0-sensitivity to F0=0.5 x BF was preserved for missing F0, but abolished by eliminating both F0 and the second harmonic. The inhibitory subfield of the frequency-receptive field was restricted to the spectral region between the preferred harmonics in F0-sensitive cells, while it was frequency unspecific in F0-insensitive cells. We conclude that (i) A1 is well organized for discrimination between harmonics and noise; (ii) pitch-height is represented along with the tonotopic axis; (iii) all aspects of the sustained neural responses to harmonic and noise stimuli are consequences of spectral filtering; and (iv) although the observed cell behavior explains some psychophysical pitch perception behaviors, such as pitch-chroma (helical pitch perception with frequency elevation), pitch-level tolerance and adaptive behavior, F0-encoding in A1 remains at the incomplete perceptual level (dominance of the third to fifth harmonics for pitch strength is unexplainable by the cell behavior).

Acoustic Stimulation↗

Distribution of combination-sensitive neurons in the ventral fringe area of the auditory cortex of the mustached bat.

1. The orientation sound (pulse) of the mustached bat, Pteronotus parnellii parnellii, consists of long constant-frequency components (CF1-4) and short frequency-modulated components (FM1-4). The auditory cortex of this bat contains several combination-sensitive areas: FM-FM, DF, VA, VF, and CF/CF. The FM-FM area consists of neurons tuned to a combination of the pulse FM1 and the echo FMn (n = 2, 3, or 4) and has an echo-delay (target-range) axis. Our preliminary anatomical studies with tritiated amino acids suggest that the FM-FM area projects to the dorsal fringe (DF) area, which in turn projects to the ventral fringe (VF) area. The aim of our study was to characterize the response properties of VF neurons and to explore the functional organization of the VF area. Acoustic stimuli delivered to the bats were CF tones, FM sounds, and their combinations mimicking the pulse emitted by the mustached bat and the echo. 2. Like the FM-FM and DF areas, the VF area is composed of three types of FM-FM combination-sensitive neurons: FM1-FM2, FM1-FM3, and FM1-FM4. These neurons show little or no response to a pulse alone, echo alone, single CF tone or single FM sound. They do, however, show a strong facilitative response to a pulse-echo pair with a particular echo delay. The essential components in the pulse-echo pair for facilitation are the FM1 of the pulse and the FMn of the echo.(ABSTRACT TRUNCATED AT 250 WORDS)

Acoustic Stimulation↗

Laminar distribution and neuronal targets of GABAergic axon terminals in cat primary auditory cortex (AI).

The form, density, and neuronal targets of presumptive axon terminals (puncta) that were immunoreactive for gamma-aminobutyric acid (GABA) or its synthesizing enzyme, glutamic acid decarboxylase (GAD), were studied in cat primary auditory cortex (AI) in the light microscope. High-resolution, plastic-embedded material and frozen sections were used. The chief results were: 1) There was a three-tiered numerical distribution of puncta, with the highest density in layer Ia, an intermediate number in layers Ib-IVb, and the lowest concentration in layers V and VI, respectively. 2) Each layer had a particular arrangement: layer I puncta were fine and granular (less than 1 micron in diameter), endings in layers II-IV were coarser and more globular (larger than 1 micron), and layer V and VI puncta were mixed in size and predominantly small. 3) The form and density of puncta in every layer were distinctive. 4) Immunonegative neurons received, in general, many more axosomatic puncta than immunopositive cells, with the exception of the large multipolar (presumptive basket) cells, which invariably had many puncta in layers II-VI. 5) The number of puncta on the perikarya of GABAergic neurons was sometimes related to the number of puncta in the layer, and in other instances it was independent of the layer. Thus, while layer V had a proportion of GABAergic neurons similar to layer IV, it had only a fraction of the number of puncta; perhaps the intrinsic projections of supragranular GABAergic cells are directed toward layer IV, as those of infragranular GABAergic neurons may be. Since puncta are believed to be the light microscopic correlate of synaptic terminals, they can suggest how inhibitory circuits are organized. Even within an area, the laminar puncta patterns may reflect different inhibitory arrangements. Thus, in layer I the fine, granular endings could contact preferentially the distal dendrites of pyramidal cells in deeper layers. The remoteness of such terminals from the spike initiation zone contrasts with the many puncta on all pyramidal cell perikarya and the large globular endings on basket cell somata. Basket cells might receive feed-forward disinhibition, pyramidal cells feed-forward inhibition, and GABAergic non-basket cells would be the target of only sparse inhibitory axosomatic input. Such arrangements imply that the actions of GABA on AI neurons are neither singular nor simple and that the architectonic locus, laminar position, and morphological identity of a particular neuron must be integrated for a more refined view of its role in cortical circuitry.

Animals↗

Neural correlates of auditory repetition priming: reduced fMRI activation in the auditory cortex.

Repetition priming refers to enhanced or biased performance with repeatedly presented stimuli. Modality-specific perceptual repetition priming has been demonstrated behaviorally for both visually and auditorily presented stimuli. In functional neuroimaging studies, repetition of visual stimuli has resulted in reduced activation in the visual cortex, as well as in multimodal frontal and temporal regions. The reductions in sensory cortices are thought to reflect plasticity in modality-specific neocortex. Unexpectedly, repetition of auditory stimuli has resulted in reduced activation in multimodal and visual regions, but not in the auditory temporal lobe cortex. This finding puts the coupling of perceptual priming and modality-specific cortical plasticity into question. Here, functional magnetic resonance imaging was used with environmental sounds to reexamine whether auditory priming is associated with reduced activation in the auditory cortex. Participants heard environmental sounds (e.g., animals, machines, musical instruments, etc.) in blocks, alternating between initial and repeated presentations, and decided whether or not each sound was produced by an animal. Repeated versus initial presentations of sounds resulted in repetition priming (faster responses) and reduced activation in the right superior temporal gyrus, bilateral superior temporal sulci, and right inferior prefrontal cortex. The magnitude of behavioral priming correlated positively with reduced activation in these regions. This indicates that priming for environmental sounds is associated with modification of neural activation in modality-specific auditory cortex, as well as in multimodal areas.

Acoustic Stimulation↗

Memory-related processing of complex sound patterns in human auditory cortex: a MEG study.

Responses of the human brain to a complex sound pattern were recorded with a 24 channel magnetometer. The sound pattern consisted of 9 successive 50 ms segments, each with a different frequency. An infrequent change in the frequency of one of the segments elicited a magnetic mismatch response (MMNm) which peaked at about 200 ms after the deviant segment onset and resembled the electrical mismatch negativity (MMN). The equivalent current dipole which best explained the MMNm was located in the supratemporal auditory cortex, suggesting that a memory trace for the sound pattern was stored in that region.

Adult↗

Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Meriones unguiculatus): 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.

Acoustic Stimulation↗

Specialization of primary auditory cortex processing by sound exposure in the "critical period".

Environmental acoustic exposure to a complex tone sequence within the critical period in infant rats resulted in the emergence of large-scale, selective changes that radically altered primary auditory cortex (A1) organization. In the sound exposure-revised A1, responses were segregated into two explicit zones representing spectrally and temporally separated lower and higher frequency tone sequence progressions. Cortical neurons between these two A1 zones were poorly driven by sound stimuli. Stimulus sequence-specific ("combination-selective") responses emerged in the A1 of exposed rats. These selective representational changes induced in the critical period persisted into adulthood. These results show that the temporal order and pace of early, repetitive postnatal auditory inputs strongly affect the emergent and enduring functional organization of A1.

Animals↗

A map of visual space induced in primary auditory cortex.

Maps of sensory surfaces are a fundamental feature of sensory cortical areas of the brain. The relative roles of afferents and targets in forming neocortical maps in higher mammals can be examined in ferrets in which retinal inputs are directed into the auditory pathway. In these animals, the primary auditory cortex contains a systematic representation of the retina (and of visual space) rather than a representation of the cochlea (and of sound frequency). A representation of a two-dimensional sensory epithelium, the retina, in cortex that normally represents a one-dimensional epithelium, the cochlea, suggests that the same cortical area can support different types of maps. Topography in the visual map arises both from thalamocortical projections that are characteristic of the auditory pathway and from patterns of retinal activity that provide the input to the map.

Animals↗

Inhibitory interactions in neuronal networks including cells of the auditory cortex and the medial geniculate body.

The use of the method of cross-correlation analysis has made it possible to identify some specific features of inhibition in neuronal networks including cells from various loci of the auditory cortex (AC) and the medial geniculate body (MGB). It was demonstrated that inhibitory MGB (AC) neurons possess "convergent" properties which are manifested in the fact one neuron simultaneously excites cells located in various loci of the AC and MGB, and "divergent" properties which are manifested in the fact that one and the same neuron may simultaneously inhibit neighboring cells and neurons from one or several AC (MGB) loci. There are short-axon inhibitory neurons in the AC which selectively act on the activity of one neighboring cell. An inhibitory AC neuron may be simultaneously included in the circuit of afferent and backward inhibition. Reciprocal connections between inhibitory MGB neurons were found. Simultaneous afferent inhibition of remote AC cells may lead to synchronization of their activity. The results make it possible to explain deviations from the principle of tonotopic organization in the AC and MGB.

Action Potentials↗

Human auditory cortex tracks task-irrelevant sound sources.

The brain organizes sound into coherent sequences, termed auditory streams. We asked whether task-irrelevant sounds would be detected as separate auditory streams in a natural listening environment that included three simultaneously active sound sources. Participants watched a movie with sound while street-noise and sequences of naturally varying footstep sounds were presented in the background. Occasional deviations in the footstep sequences elicited the mismatch negativity (MMN) event-related potential. The elicitation of MMN showed that the regular features of the footstep sequences had been registered and their violations detected, which could only occur if the footstep sequence had been detected as a separate auditory stream. Our results demonstrate that sounds are organized into auditory streams irrespective of their relevance to ongoing behavior.

Acoustic Stimulation↗

Evoked potentials of the human auditory cortex: sensitive to the harmonic series?

Cortically generated auditory evoked potentials (N1 and P2) were recorded to frequency changes of harmonic and inharmonic complex tones comprising four sinusoidal components. The responses obtained when the frequencies suddenly became stationary after a period of 16/s changes were significantly shorter in latency when the frequencies were harmonically related, possibly implying a process of periodicity detection.

Adult↗

Receptive-field plasticity in the adult auditory cortex induced by Hebbian covariance.

The goal of this experiment was to evaluate the role of cellular interactions postulated by the Hebbian, or covariance, hypothesis in the induction of receptive-field (RF) plasticity in the adult auditory cortex (ACx). This was accomplished by determining whether a "covariance treatment" (see below) was sufficient to induce RF plasticity without behavioral experiences that normally induce such plasticity. During the covariance treatment (conducted in urethane-anesthetized adult guinea pigs), one tone was paired with excitatory juxtacellular current, applied to a single postsynaptic cell in the primary ACx. Excitatory current increased postsynaptic discharge, thereby increasing covariance between activity of the postsynaptic cell and its afferents that were activated by the tone. In alternation, within the same cell a second, different tone was paired with inhibitory juxtacellular current, decreasing covariance between the postsynaptic cell and afferents activated by the second tone. After treatment, responses to tones associated with increased covariance strengthened significantly relative to tones associated with decreased covariance, as predicted by the Hebbian hypothesis. This occurred in 7 of 22 (32%) cells undergoing 120 pairing trials, but in only 4 of 38 (11%) cells undergoing 60 trials. Fewer than 5% of cells showed significant effects opposite those predicted by the hypothesis. Significant plasticity lasted > or = 15 min. Probability of plasticity was significantly higher when the cortical electroencephalogram was nonsynchronized during treatment (5/9 cells) than when synchronized (2/13 cells). These findings support the role of presynaptic-postsynaptic covariance processes in the induction of adult neocortical RF plasticity and suggest that factors associated with cortical state "gate" such plasticity.

Acoustic Stimulation↗

Neural changes in cat auditory cortex after a transient pure-tone trauma.

Here we present the changes in cortical activity occurring within a few hours after a 1-h exposure to a 120-dB SPL pure tone (5 or 6 kHz). The changes in primary auditory cortex of 16 ketamine-anesthetized cats were assessed by recording, with two 8-microelectrode arrays, from the same multiunit clusters before and after the trauma. The exposure resulted in a peripheral threshold increase that stabilized after a few hours to on average 40 dB in the frequency range of 6-32 kHz, as measured by the auditory brain stem response. The trauma induced a shift in characteristic frequency toward lower frequencies, an emergence of new responses, a broadening of the tuning curve, and an increase in the maximum of driven discharges. In addition, the onset response after the trauma was of shorter duration than before the trauma. The results suggest the involvement of both a decrease and an increase in inhibition. They are discussed in terms of changes in central inhibition and its implications for tonotopic map plasticity.

Acoustic Stimulation↗

Amplitude spectrum representation in the Doppler-shifted-CF processing area of the auditory cortex of the mustache bat.

The mustache bat, Pteronotus parnellii rubiginosus, emits orientation sounds containing a long constant-frequency (CF) component that is ideal for echo detection and Doppler shift measurement. About 30 percent of the primary auditory cortex of this bat is chiefly devoted to processing the second harmonic of the CF component in Doppler-shifted echoes. In this Doppler-shifted-CF processing area, single neurons recorded in any electrode penetration perpendicular to the cortical surface have nearly identical best frequencies and best amplitudes (or best pressure levels) at which the neurons show maximum excitation. The best frequency and best amplitude vary systematically with the location of the neurons in the cerebral cortex, so that there are tonotopic and "amplitopic" representation axes, which are radial and eccentric, respectively. In other words, the best-frequency and best-amplitude contours are eccentric and radial, respectively. The amplitude spectrum of a signal is thus represented in the coordinates of amplitude and frequency parallel to the cortical surface. This amplitude spectrum representation is disproportionate according to perceptual significance, so that a signal of 61.5 to 62.0 kilohertz and 30 to 50 decibels SPL (sound pressure level) is projected to a larger area than other signals. Just outside this Doppler-shifted-CF processing area, neurons are found which are specialized for responding to a particular information-bearing element or a particular combination of information-bearing elements in orientation sounds and echoes consisting of CF and frequency-modulated components.

Animals↗

Multiple combination-sensitive neurons in the auditory cortex of the mustached bat.

The mustached bat, Pteronotus parnellii, emits biosonar pulses consisting of four constant-frequency (CF(1-4)) and four frequency-modulated (FM(1-4)) components. The FM-FM area of its auditory cortex consists of three subdivisions, containing either FM(1)-FM(2), FM(1)-FM(3) or FM(1)-FM(4) combination-sensitive neurons. The FM-FM area also contains 'multiple combination-sensitive' neurons: FM(1)-FM(2,3), FM(1)-FM(3,4), FM(1)-FM(2,4), and FM(1)-FM(2,3,4) neurons. All FM-FM neurons are tuned to a time delay (echo delay) of FM(n) (n=2-4) from FM(1). In the present study, we made the following four major findings. (1) Multiple combination-sensitive neurons show the strongest response to a combination of more than two signal elements. (2) Multiple combination-sensitive neurons are located in about 100 microm wide bands at the boundaries between two adjacent subdivisions of the FM-FM area. (3) Iso-best-delay contour lines across the three single combination-sensitive subdivisions are not interrupted by multiple combination-sensitive bands. (4) Each subdivision of the FM-FM area has frequency-vs.-frequency coordinates in terms of best FM(1) and best FM(n) frequencies for facilitation, although such coordinates were not obtained with single tone bursts.

Acoustic Stimulation↗

Canadian Association of Neuroscience Review: development and plasticity of the auditory cortex.

The functions of the cerebral cortex are predominantly established during the critical period of development. One obvious developmental feature is its division into different functional areas that systematically represent different environmental information. This is the result of interactions between intrinsic (genetic) factors and extrinsic (environmental) factors. Following this critical period, the cerebral cortex attains its adult form but it will continue to adapt to environmental changes. Thus, the cerebral cortex is constantly adapting to the environment (plasticity) from its embryonic stages to the last minute of life. This review details important factors that contribute to the development and plasticity of the auditory cortex. The instructive role of thalamocortical innervation, the regulatory role of cholinergic projection of the basal forebrain and the potential role of the corticofugal modulation are presented.

Acetylcholine↗