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Analysis of dynamic spectra in ferret primary auditory cortex. I. Characteristics of single-unit responses to moving ripple spectra.

1. Auditory stimuli referred to as moving ripples are used to characterize the responses of both single and multiple units in the ferret primary auditory cortex. Moving ripples are broadband complex sounds with a sinusoidal spectral profile that drift along the logarithmic frequency axis at a constant velocity. 2. Neuronal responses to moving ripples are locked to the phase of the ripple, i.e., they exhibit the same periodicity as that of the moving ripple profile. Neural responses are characterized as a function of ripple velocity (temporal property) and ripple frequency (spectral property). Transfer functions describing the response to these temporal and spectral modulations are constructed. Temporal transfer functions are inverse Fourier transformed to obtain impulse response functions that reflect the cell's temporal characteristics. Ripple transfer functions are inverse Fourier transformed to obtain the response field, a measure analogous to the cell's response area. These operations assume linearity in the cell's response to moving ripples. 3. Transfer functions and other response functions are shown to be fairly independent on the overall level or depth of modulation of the ripple stimuli. Only downward moving ripples were used in this study. 4. The temporal and ripple transfer functions are found to be separable, in that their shapes remain unchanged for different test parameters. Thus ripple transfer functions and response fields remain statistically similar in shape (to within an overall scale factor) regardless of the ripple velocity or whether stationary or moving ripples are used in the measurement. The same stability in shape holds for the temporal transfer functions and the impulse response functions measured with different ripple frequencies. Separability implies that the combined spectrotemporal transfer function of a cell can be written as the product of a purely ripple and a purely temporal transfer functions, and thus that the neuron can be computationally modeled as processing spectral and temporal information in two separate and successive stages. 5. The ripple parameters that characterize cortical cells are distributed somewhat evenly, with the characteristic ripple frequencies ranging from 0.2 to > 2 cycles/octave and the characteristic angular frequency typically ranging from 2 to 20 Hz. 6. Many responses exhibit periodicities in the spectral envelope of the stimulus. These periodicities are of two types. Slow rebounds, not found in the spectral envelope, and with a period of approximately 150 ms, appear with various strengths in approximately 30% of the cells. Fast regular firings with interspike intervals of approximately 10 ms are much less common and appear to correspond to interactions between the component tones that make up a ripple.

Acoustic Stimulation↗

[The interaction of neurons characterized by a tonic reaction to sound with other neurons in the cat auditory cortex].

Interaction of neurons with tonic response to sound with adjacent or distant (approximately 400-500 micrograms) cortex neurons was studied in acute experiments on 15 immobilized cats using a method of the cross-correlation analysis. A presence of synchronizing excitatory input common for the cells has been revealed in 26 pairs (72%) on the cross-correlograms. The results of the cross-correlation analysis in five pairs of neurons show mono- or polysynaptic excitatory effect of a tonic neuron to impulse activity of another neuron. Negative correlation indicative of the inhibitory influence of tonic neurons on impulse responses of other neurons of the same or adjacent auditory cortex column is revealed in five pairs of neurons, but the inhibitory influences may be considered as monosynaptic ones only in 3 pairs of these neurons (latency of interaction 1.0-1.5 ms). The data obtained permit concluding that the group of neurons characterized by tonic response to sound is a heterogeneous one in the functional respect. An assumption that some neurons of the tonic type are inhibitory interneurons of the auditory cortex, other excitatory ones is under discussion.

Acoustic Stimulation↗

Electromagnetic responses of the human auditory cortex generated by sensory-memory based processing of tone-frequency changes.

Event-related brain potentials (ERPs) and magnetoencephalographic (MEG) responses to infrequent ('deviant') tones occurring among frequent ('standard') tones of different pitch were compared with responses to rare tones presented alone. The subjects were to ignore the tones. Deviant tones elicited the mismatch negativity (MMN) and its MEG counterpart (MMNm), while the rare tones delivered alone elicited a larger N1 and its MEG counterpart (N1m) than did standard tones. Source modeling of MEG responses indicated a difference in auditory-cortex source locations between the MMNm to deviant tones and the enhanced N1m to the rare tones presented alone. Thus, the MMN/MMNm is elicited by infrequent sounds only when they occur among frequent sounds. This supports the idea that a sensory-memory trace formed in the auditory cortex by preceding repetitive sounds is a necessary precondition for MMN/MMNm elicitation.

Acoustic Stimulation↗

Differential synaptic processing separates stationary from transient inputs to the auditory cortex.

Sound features are blended together en route to the central nervous system before being discriminated for further processing by the cortical synaptic network. The mechanisms underlying this synaptic processing, however, are largely unexplored. Intracortical processing of the auditory signal was investigated by simultaneously recording from pairs of connected principal neurons in layer II/III in slices from A1 auditory cortex. Physiological patterns of stimulation in the presynaptic cell revealed two populations of postsynaptic events that differed in mean amplitude, failure rate, kinetics and short-term plasticity. In contrast, transmission between layer II/III pyramidal neurons in barrel cortex were uniformly of large amplitude and high success (release) probability (Pr). These unique features of auditory cortical transmission may provide two distinct mechanisms for discerning and separating transient from stationary features of the auditory signal at an early stage of cortical processing.

Action Potentials↗

Laminar connections of the cat's auditory cortex.

The retrograde and the anterograde transport of horseradish peroxidase were used to study the connections established by cells in different layers of the cat's primary auditory cortex (AI). Injections of peroxidase into the medial geniculate body show that pyramidal cells in layers V and VI of AI are the sources of the corticothalamic projections. Large pyramidal cells in the outer rim of layer V also send their axons to the inferior colliculus, and it is possible that some of these cells have axons that branch to innervate both the inferior colliculus and the medial geniculate body. Cells in AI that give rise to callosal axons lie principally in layers III and VI. The callosal neurons are found in irregular clusters as wide as 1100 microgram separated by spaces that contain relatively few callosal neurons. Experiments utilizing the anterograde transport of peroxidase show that callosal terminals are found in bands running from layers VI through I. These bands are about 500 microgram in width, and the terminals seem most densely packed in layers II and III. Since the dimensions of the cell clusters and bands of callosal terminals are not the same, it is likely that not all zones which give rise to callosal axons also receive them. The bands of callosal terminals labeled by orthograde transport may be seen in the same section along with the cell bodies labeled by retrograde transport, and the two zones of label are clearly not coextensive. Complete reciprocity, therefore, seems to be absent in the callosal auditory pathway.

Animals↗

Projections of auditory cortex upon the thalamus and midbrain in the owl monkey.

Two tonotopically organized cortical fields, the primary (AI) and the rostral (R) fields, comprise the core of auditory cortex in the owl monkey. Injections of tritiated proline were made into each of these fields to determine their efferent projections using autoradiographic methods. Both AI and R project to the principal and magnocellular divisions of the medial geniculate body. In addition, R projects to the posterior part of the dorsal division of the medial geniculate. AI sends axons to the dorsomedial region and laminated portion of the central nucleus of the inferior colliculus. Labeling in the central nucleus following AI injections appears as a band of silver grains oriented parallel to isofrequency contours. Axons from R terminate in the dorsomedial region of the central nucleus of the inferior colliculus and in the pericentral and external nuclei of the inferior colliculus. In addition, the rostral field projects to a small area of the medial pulvinar just anterior to the brachium of the superior colliculus.

Animals↗

Multivariate receptive field mapping in marmoset auditory cortex.

We describe a novel method for estimation of multivariate neuronal receptive fields that is based on least-squares (LS) regression. The method is shown to account for the relationship between the spike train of a given neuron, the activity of other neurons that are recorded simultaneously, and a variety of time-varying features of acoustic stimuli, e.g. spectral content, amplitude, and sound source direction. Vocalization-evoked neuronal responses from the marmoset auditory cortex are used to illustrate the method. Optimal predictions of single-unit activity were obtained by using the recent-time history of the target neuron and the concurrent activity of other simultaneously recorded neurons (R: 0.82 +/- 0.01, approximately 67% of variance). Predictions based on ensemble activity alone (R: 0.63 +/- 0.18) were equivalent to those based on the combination of ensemble activity and spectral features of the vocal calls (R: 0.61 +/- 0.24). This result suggests that all information derived from the spectrogram is embodied in ensemble activity and that there is a high level of redundancy in the marmoset auditory cortex. We also illustrate that the method allows for quantification of relative and shared contributions of each variable (spike train, spectral feature) to predictions of neuronal activity and describe a novel "neurolet" transform that arises from the method and that may serve as a tool for computationally efficient processing of natural sounds.

Acoustic Stimulation↗

Maturational aspects of periodicity coding in cat primary auditory cortex.

The click-following responses for single units in the primary auditory cortex of the cat were explored as a function of age. Recordings were obtained in kittens from 9-53 days of age and assembled in four age groups; 10-15 days, 16-21 days, 22-27 days and 30-60 days. Age group means were compared to results obtained in adult cats. The stimulus consisted of one second long click trains presented every three seconds with click rates ranging from 1-32 clicks per second. The response was characterized by entrainment, rate Modulation Transfer Function (rMTF), vector strength (VS) and temporal Modulation Transfer Function (tMTF). Maturational effects on periodicity coding comprised changes in overall responsiveness as well as click-rate dependent changes. The number of spikes elicited by single stimuli increased on average 3-fold between the second post-natal week and adulthood, probably as a result of more efficient synapses in the central auditory pathway and some improvement in thresholds. Adaptation became less pronounced with age; neurons started to respond to the later clicks in the 8/s and 16/s click trains from the third post natal week on. By the end of the first post-natal month the click following responses resembled the adult ones qualitatively, however, increased firing rates and spontaneous rates together with rebound responses continued to produce quantitative differences between the 30-60 days olds and the adults. Limiting rates for the tMTF (50% of the response at 1/s) increased from 6 Hz in the 10-15 day old to 12 Hz in adults. The decrease in the duration of the post-activation suppression coupled with the increased response with age to trains with higher click rates suggested that the maturation of inhibitory processes in the cortex play a major role in this rate dependence.

Acoustic Stimulation↗

Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex.

We examined the effect of unilateral restricted cochlear lesions in adult cats on the topographic representations ("maps") of the lesioned and unlesioned cochleas in the primary auditory cortex (AI) contralateral to the lesioned cochlea. Frequency (tonotopic) maps were derived by conventional multineuron mapping procedures in anesthetized animals. In confirmation of a study in adult guinea pigs (Robertson and Irvine [1989] J. Comp. Neurol. 282:456-471), we found that 2-11 months after the unilateral cochlear lesion the map of the lesioned cochlea in the contralateral AI was altered so that the AI region in which frequencies with lesion-induced elevations in cochlear neural sensitivity would have been represented was occupied by an enlarged representation of lesion-edge frequencies (i.e., frequencies adjacent to those with elevated cochlear neural sensitivity). Along the tonotopic axis of AI the total representation of lesion-edge frequencies could extend up to approximately 2.6 mm rostal to the area of normal representation of these frequencies. There was no topographic order within this enlarged representation. Examination of threshold sensitivity at the characteristic frequency (CF, frequency to which the neurons were most sensitive) in the reorganized regions of the map of the lesioned cochlea established that the changes in the map reflected a plastic reorganization rather than simply reflecting the residue of prelesion input. In contrast to the change in the map of the lesioned contralateral cochlea, the map of the unlesioned ipsilateral cochlea did not differ from those in normal animals. Thus, in contrast to the normal very good congruency between ipsilateral and contralateral AI maps, in the lesioned animals ipsilateral and contralateral maps differed in the region of AI in which there had been a reorganization of the map of the lesioned cochlea. Outside the region of contralateral map reorganization, ipsilateral and contralateral AI maps remained congruent within normal limits. The difference between the two maps in the region of contralateral map reorganization suggested, in light of the physiology of binaural interactions in the auditory pathway, that the cortical reorganization reflected subcortical changes. Finally, response properties of neuronal clusters within the reorganized map of the lesioned cochlea were compared to normative data with respect to threshold sensitivity at CF, the size of frequency "response areas," and response latencies. In the majority of cases, CF thresholds were similar to normative data. The frequency "response areas" were slightly less sharply tuned than normal, but not significantly. Response latencies were significantly shorter than normal in three animals and significantly longer in one animal.

Animals↗

Onset and offset responses from inferior colliculus and auditory cortex to paired noisebursts: inner hair cell loss.

Thirteen adult chinchillas were anesthetized with ketamine/acepromazine and tungsten electrodes were placed in the right inferior colliculus (IC) and auditory cortex (AC). A reference electrode was implanted in the anterior cranium. Following a recovery period, AC and IC responses to left ear stimulation were obtained from unanesthetized animals resting in a passive restraint inside a sound-attenuating booth. After the first recording, the animals were injected with carboplatin (75 mg/kg). Four to five weeks later, a second recording was made. Stimuli were 50 ms duration (0 ms rise and fall time), 80 dB SPL noiseburst pairs. In one group of seven animals, the gap time varied from 1 to 64 ms. In a second group of six animals, the gap time ranged from 0.25 to 64 ms in order to determine gap threshold. The responses were amplified (10000x) and filtered from 10 to 3000 Hz. Each response was the average of 100 stimulus presentations. The dependent variables were the latency of the initial positive peak and the amplitude of the response from initial positive peak to the following negativity. Following the second recording, all animals were sacrificed, the cochleas harvested, and cochleograms were obtained by counting outer hair cells (OHCs) and inner hair cells (IHCs). For the onset response to the second noiseburst of each pair, response amplitudes decreased and latencies increased with decreasing gap time. For a 64 ms gap time, the IC response approached the latencies and amplitudes seen for the onset response to the single noiseburst or first noiseburst in the pair (herein called "baseline" values), while the AC response latency approached baseline values, but AC amplitude did not. Interestingly, the offset responses to the first noiseburst were not present at gaps of less than 8 ms, while the onset responses to the second noiseburst were typically present at gaps of 1-2 ms. Cochleograms revealed a normal (or near-normal) complement of OHCs, and IHC loss averaging roughly 30-40% in apical regions and increasing to 60-70% in more basal regions (compared to normative data). Following carboplatin, the latencies of IC onset responses were delayed by several tenths of a millisecond, with the greatest pre- versus post-carboplatin latency shift occurring at short noiseburst gaps. AC response latencies were largely unaffected by carboplatin. IC onset response amplitudes were reduced following carboplatin, while AC onset responses were similar to pre-carboplatin values. IC offset response latencies to the first noiseburst were increased post-carboplatin, while AC offset response latencies varied little from pre-carboplatin values. IC and AC offset response amplitudes to the first noiseburst were decreased post-carboplatin.

Acoustic Stimulation↗

Functional organization of the auditory cortex: maps and mechanisms.

Recent studies have led to a better understanding of several aspects of the organization and physiological mechanisms involved in the processing of information in the auditory cortex. A wide range of approaches have revealed new information regarding the histochemistry, cortico-cortical connections, single-unit physiology, and functional spatial organization, as well as mechanisms and effects of representational and learning-induced cortical plasticity.

Animals↗

Responses to linear and logarithmic frequency-modulated sweeps in ferret primary auditory cortex.

Multi-unit responses to frequency-modulated (FM) sweeps were studied in the primary auditory cortex of ferrets using six different stimulation paradigms. In particular, the differences between the responses to linear FM sweeps (where frequency changes linearly with time) and logarithmic FM sweeps (where frequency changes exponentially with time) were emphasized. Some general features of the responses to FM sweeps are independent of the exact details of the frequency trajectory. Both for linear and for logarithmic FM sweeps, a short burst of spikes occurred when the sweep reached a triggering frequency close to the best frequency of the cluster. The neuronal preference for FM velocity was also independent of frequency trajectory. Thus, clusters that responded best to slow logarithmic FM also preferred slow linear FM and vice versa. Consequently, topographic distributions of velocity preference were roughly independent of the stimulation paradigm. Other characteristics of the responses, however, depended on the exact details of the frequency trajectory. A significant number of clusters showed large differences in directional sensitivity between linear and logarithmic FM sweeps; these differences depended on the velocity preference of the clusters in some paradigms but not in others. Consequently, topographic distributions of directional sensitivity differed between linear and logarithmic paradigms. In conclusion, some characteristics of cluster responses to FM sweeps depend on the exact details of the stimulation paradigm and are not 'invariants' of the cluster.

Acoustic Stimulation↗

Isofrequency band-like zones of activation revealed by optical imaging of intrinsic signals in the cat primary auditory cortex.

Neurons of similar frequency preference are arranged in isofrequency bands (IFBs) across the primary auditory cortex (AI) of many mammals. Across the AI of the cat, one of the most frequently studied species for auditory anatomy and function, we demonstrate IFB-like responses using optical imaging of intrinsic signals (OIS). Optically defined activations were extensively elongated along the dorsoventral axis of AI (the ratio of the major and minor axes was approximately 2:1), and systematically shifted as a function of stimulus frequency. The elongation of this IFB-like zone was more conspicuous at higher frequencies. In the ventral sector of the imaged field, the IFB-like zones of activation evoked at different pure tone frequencies tended to overlap extensively. Electrophysiological recording from loci within the optically defined zones of activation revealed matched responses to the frequencies used for optical imaging at 65% of these loci. The dorsoventral orientation of these zones of activation was also closely matched with the orientation of tangentially spreading intrinsic axon terminals, as revealed anatomically. The visualization of IFB-like architecture and tonotopic organization by OIS provides a basic framework for investigating the relationships of different spectral channels and between multiple acoustic parameters at a neuronal population level.

Acoustic Stimulation↗

Hebbian-like functional plasticity in the auditory cortex of the behaving monkey.

In this study, the necessary conditions, including those related to behavior, for lasting modifications to occur in correlated activity ('functional plasticity') were examined in the behaving monkey. Previously, in-vitro studies of neuronal plasticity yielded important information about possible mechanisms of synaptic plasticity, but could not be used to test their functionality in the intact, behaving brain. In-vivo studies usually focused on analysis of the responsiveness of single cells, but did not examine interactions between pairs of neurons. In this study, we combined the two approaches. This was achieved by recording extracellularly and simultaneously the spike activity of several single cells in the auditory cortex of the behaving monkey. The efficacy of neuronal interactions was estimated by measuring the correlation between firing times of pairs of single neurons. Using acoustic stimuli, a version of cellular conditioning was applied when the monkey performed an auditory discrimination task and when it did not. We found that: (i) functional plasticity is a function of the change in correlation, and not of the correlation or covariance per se, and (ii) functional plasticity depends critically on behavior. During behavior, an increase in the correlation caused a short-lasting strengthening of the neuronal coupling efficacy, and a decrease caused a short-lasting weakening. These findings indicate that neuronal plasticity in the auditory cortex obeys a version of Hebb's associative rule under strong behavioral control, as predicted by Thorndike's "Law of Effect".

Acoustic Stimulation↗

A direct demonstration of functional specialization within motion-related visual and auditory cortex of the human brain.

BACKGROUND: Physiological studies of the macaque brain have shown that there is a large expanse of visual cortex, the V5 complex, which is specialized for visual motion, and that several areas within V5 are specialized for different kinds of visual motion. In continuing work on motion-related visual cortex, we wished to chart the specialized visual motion areas in the human brain and to determine their anatomical relationship. Human subjects viewed different motion displays, and the cortical location of the increased activity produced by each stimulus was recorded. The technique of functional magnetic resonance imaging (fMRI) was used, in order to image the same subjects repeatedly. RESULTS: We found that each of the three motion stimuli activated specific parts of the V5 complex. These sites of activation overlap with V5 and, to a smaller extent, with each other. Unexpectedly, the three motion stimuli also activated neighbouring, but nonoverlapping, regions of auditory cortex that are normally activated by the perception of speech. CONCLUSIONS: The three sites of activation produced by the visual motion stimuli occupy adjacent territories within the V5 complex. Components of the V5 complex are specifically connected to regions within auditory cortex.

Auditory Cortex↗

Decoding of auditory cortex signals with a LAMSTAR neural network.

OBJECTIVES: Each neuron has a specific set of stimuli, which it preferentially responds to (the receptive field of the neuron). For implantable cortical prosthetic devices specific points of the cortex (or groups of neurons) have to be stimulated to create perceptions of sensory stimulus with specific attributes (such as frequency, temporal characteristics, etc). Such applications would need real time decoding of signals. Previously mathematical techniques, such as computing the receptive field (using electrophysiology data) and artificial neural networks (Kohonen network or SOM and back propagation network) have been used to decode neural signals. METHODS: A Large Adaptive Memory Storage and Retrieval (LAMSTAR) neural-network-based decoder was designed to decode responses recorded from neurons in the auditory cortex. It was designed to identify the frequency of the tonal stimuli that elicited a particular discharge rate pattern recorded on two channels of a tungsten wire electrode array. RESULTS: The network functioned efficiently as a decoder with 100% accuracy for the small sample of stimulus-response data used. DISCUSSION: The results show that the network is effective in studying the functional organization of the auditory cortex and other sensory systems. Depending on the input sub-word, information about the kind of stimuli that activates particular parts of the sensory cortex can be studied.

Acoustic Stimulation↗

A complex tone code in the auditory cortex.

In the search for an objective measure of a biologically meaningful encoding scheme for cochlear implants, we recorded responses to tones from the alert auditory cortex. Neurons in the primary auditory field (A1) are typically characterized by filter characteristics resembling those of eighth nerve afferent fibers (filter neurons). In contrast, a different class of neurons has been found thus far only outside of the cochleotopic A1 array. These cells are sharply tuned to pure tones, and corresponding fundamental frequencies of harmonic complexes (F0 neurons). Thus these cells are specific for various tones of the same pitch. Sharpened pure- and complex-tone tuning can be accounted for by lateral inhibition. Time patterns for tonal and noise responses can vary dramatically.

Acoustic Stimulation↗

Spatial versus object feature processing in human auditory cortex: a magnetoencephalographic study.

The human visual system is divided into two pathways specialized for the processing of either objects or spatial locations. Neuroanatomical studies in monkeys have suggested that a similar specialization may also divide auditory cortex into two such pathways. We used the identical stimulus material in two experimental sessions in which subjects had to either identify auditory objects or their location. Magnetoencephalograms were recorded and M100 dipoles were fitted into individual brain models. In the right hemisphere, the processing of auditory spatial information lead to more lateral activations within the temporal plane while object identification lead to more medial activations. These findings suggest that the human auditory system processes object features and spatial features in distinct areas.

Acoustic Stimulation↗