Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation: IV. Activation pattern for sinusoidal stimulation

Patterns of threshold distributions for single-cycle sinusoidal electrical stimulation and single pulse electrical stimulation were compared in primary auditory cortex of the adult cat. Furthermore, the effects of auditory deprivation on these distributions were evaluated and compared across three groups of adult cats. Threshold distributions for single and multiple unit responses from the middle cortical layers were obtained on the ectosylvian gyrus in an acutely implanted animal; 2 wk after deafening and implantation (short-term group); and neonatally deafened animals implanted following 2-5 yr of deafness (long-term group). For all three cases, we observed similar patterns of circumscribed regions of low response thresholds in the region of primary auditory cortex (AI). A dorsal and a ventral region of low response thresholds were found separated by a narrow, anterior-posterior strip of elevated thresholds. The ventral low-threshold regions in the short-term group were cochleotopically arranged. By contrast, the dorsal region in the short-term animals and both low-threshold regions in long-term deafened animals maintained only weak cochleotopicity. Analysis of the spatial extent of the low-threshold regions revealed that the activated area for sinusoidal stimulation was smaller and more circumscribed than for pulsatile stimulation for both dorsal and ventral AI. The width of the high-threshold ridge that separated the dorsal and ventral low-threshold regions was greater for sinusoidal stimulation. Sinusoidal and pulsatile threshold behavior differed significantly for electrode configurations with low and high minimum thresholds. Differences in threshold behavior and cortical response distributions between the sinusoidal and pulsatile stimulation suggest that stimulus shape plays a significant role in the activation of cortical activity. Differences in the activation pattern for short-term and long-term deafness reflect deafness-induced reorganizational changes based on factors such as differences in excitatory and inhibitory balance that are affected by the stimulation parameters.     

Auditory detection and discrimination in deaf cats: psychophysical and neural thresholds for intracochlear electrical signals.

More than 30,000 hearing-impaired human subjects have learned to use cochlear implants for speech perception and speech discrimination. To understand the basic mechanisms underlying the successful application of contemporary speech processing strategies, it is important to investigate how complex electrical stimuli delivered to the cochlea are processed and represented in the central auditory system. A deaf animal model has been developed that allows direct comparison of psychophysical thresholds with central auditory neuronal thresholds to temporally modulated intracochlear electrical signals in the same animals. Behavioral detection thresholds were estimated in neonatally deafened cats for unmodulated pulse trains (e.g., 30 pulses/s or pps) and sinusoidal amplitude-modulated (SAM) pulse trains (e.g., 300 pps, SAM at 30 Hz; 300/30 AM). Animals were trained subsequently in a discrimination task to respond to changes in the modulation frequency of successive SAM signals (e.g., 300/8 AM vs. 300/30 AM). During acute physiological experiments, neural thresholds to pulse trains were estimated in the inferior colliculus (IC) and the primary auditory cortex (A1) of the anesthetized animals. Psychophysical detection thresholds for unmodulated and SAM pulse trains were virtually identical. Single IC neuron thresholds for SAM pulse trains showed a small but significant increase in threshold (0.4 dB or 15.5 microA) when compared with thresholds for unmodulated pulse trains. The mean difference between psychophysical and minimum neural thresholds within animals was not significant (mean = 0.3 dB). Importantly, cats also successfully discriminated changes in the modulation frequencies of the SAM signals. Performance on the discrimination task was not affected by carrier rate (100, 300, 500, 1,000, or 1,500 pps). These findings indicate that 1) behavioral and neural response thresholds are based on detection of the peak pulse amplitudes of the modulated and unmodulated signals, and 2) discrimination of successive SAM pulse trains is based on temporal resolution of the envelope frequencies. Overall, our animal model provides a robust framework for future studies of behavioral discrimination and central neural temporal processing of electrical signals applied to the deaf cochlea by a cochlear implant.     

Neural responses in primary auditory cortex mimic psychophysical, across-frequency-channel, gap-detection thresholds

Responses of single- and multi-units in primary auditory cortex were recorded for gap-in-noise stimuli for different durations of the leading noise burst. Both firing rate and inter-spike interval representations were evaluated. The minimum detectable gap decreased in exponential fashion with the duration of the leading burst to reach an asymptote for durations of 100 ms. Despite the fact that leading and trailing noise bursts had the same frequency content, the dependence on leading burst duration was correlated with psychophysical estimates of across frequency channel (different frequency content of leading and trailing burst) gap thresholds in humans. The duration of the leading burst plus that of the gap was represented in the all-order inter-spike interval histograms for cortical neurons. The recovery functions for cortical neurons could be modeled on basis of fast synaptic depression and after-hyperpolarization produced by the onset response to the leading noise burst. This suggests that the minimum gap representation in the firing pattern of neurons in primary auditory cortex, and minimum gap detection in behavioral tasks is largely determined by properties intrinsic to those, or potentially subcortical, cells.     

Deficits of non-verbal auditory perception in postlingually deaf humans using cochlear implants

Temporal integration in the time domain of a few seconds was investigated with a subjective accentuation paradigm in 11 monochannel cochlear implant users, who showed auditory comprehension deficits. While listening to metronome beats generated at various frequencies, patients were asked to accentuate mentally every n-th beat and create an individual rhythmic pattern. The extent of temporal integration was defined as the duration of perceptual units consisting of subjectively grouped beats at particular metronome frequencies. The results indicate that there is reduced capacity for temporal integration in implant recipients, particularly for lower metronome frequencies, in comparison to normally hearing. These observations point to the coincidence of specific temporal processing disorders and deficits in auditory comprehension after cochlear implantation.     

Influence of auditory localization cues on neuronal activity in the auditory thalamus of the cat

1. The response properties of auditory thalamic neurons to the two major localization cues characterizing the azimuth of sound sources in the horizontal plane were investigated in cats. Single-unit responses to auditory stimuli (white noise and tones) presented with interaural phase differences (IPD) or interaural intensity differences (IID) were studied. 2. The proportion of neurons in the medial geniculate body that were sensitive to the localization cues tested was 28% for IPD (n = 253) and 37% for IID (n = 65). Half of the IID-sensitive units were also sensitive to IPD, but when the range of IPDs and IIDs to which each unit responded was converted to the sound-source locations that would generate those ranges they did not always correspond to overlapping azimuth angles. 3. The changes in discharge rate in response to the two localization cues occurred over very broad IPD and IID ranges. If this activity is involved in the representation of acoustic space, then the responses of individual neurons do not provide fine spatial tuning. 4. Contralateral and ipsilateral ear leads were represented in a continuous manner by the maximum discharge rate of IPD-sensitive units. On the other hand, units that were sensitive to IIDs were activated over one of two delimited ranges of IIDs. The first corresponded to IID combinations in which the stimulus was presented at a higher intensity in one ear than in the other (for 15/17 units the contralateral one); these were the lateralized intensity response field units. The second are the centered intensity response field units, whose responses were maximal when the intensity was equal in both ears and decreased when IIDs were introduced.     

Human intramuscular and cutaneous pain: psychophysical comparisons

 We used psychophysical methods to compare the central processing of nociceptive inputs from skin and muscle in ten normal humans. Both intramuscular electrical and infrared CO₂ laser cutaneous stimulation showed increasing but decelerating (downward concave) stimulus-response curves and similar temporal summation characteristics. Intramuscular stimulation was rated significantly more unpleasant than cutaneous stimulation. The results are consistent with a common mode of central nociceptive processing for skin and muscle pain intensity but suggest a relatively larger activation of affective mechanisms by muscle afferents. Received: 30 July 1996 / Accepted: 28 November 1996     

Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. III. Activation patterns in short- and long-term deafness

The effects of auditory deprivation on the spatial distribution of cortical response thresholds to electrical stimulation of the adult cat cochlea were evaluated. Threshold distributions for single- and multiple-unit responses from the middle cortical layers were obtained on the ectosylvian gyrus in three groups of animals: adult, acutely implanted animals ("acute group"); adult animals, 2 wk after deafening and implantation ("short-term group"); adult, neonatally deafened animals ("long-term group") implanted after 2-5 years of deafness. For all three groups, we observed similar patterns of circumscribed regions of low response thresholds in the region of primary auditory cortex (AI). A dorsal and a ventral region of low response thresholds were found separated by a narrow, anterior-posterior strip of elevated thresholds. The two low-threshold regions in the acute and the short-term group were arranged cochleotopically. This was reflected in a systematic shift of the cortical locations with minimum thresholds as a function of cochlear position of the radial and monopolar stimulation electrodes. By contrast, the long-term deafened animals maintained only weak or no signs of cochleotopicity. In some cases of this group, significant deviations from a simple tri-partition of the dorsoventral axis of AI was observed. Analysis of the spatial extent of the low-threshold regions revealed that the activated area in acute cases was significantly smaller than the long- and the short-term cases for both dorsal and ventral AI. There were no significant differences in the rostrocaudal extent of activation between long- and short-term deafening, although the total activated area in the short-term cases was larger than in long-term deafened animals. The width of the narrow high-threshold ridge that separated the dorsal and ventral low-threshold regions was the widest for the acute cases and the narrowest for the short-term deafened animals. The findings of relative large differences in cortical response distributions between the acute and short-term animals suggests that the effects observed in long-term deafened animals are not solely a consequence of loss of peripheral innervation density. The effects may reflect electrode-specific effects or reorganizational changes based on factors such as differences in excitatory and inhibitory balance.     

The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Electron microscopy

We have studied the posterior division of the anteroventral cochlear nucleus, where the cochlear nerve root enters the brain, in the cat. In Nissl preparations, this region contains two types of neuronal cell bodies: globular and multipolar. The two types can be identified in the electron-microscope by comparing Nissl substance and rough endoplasmic reticulum. Globular cell bodies receive many synaptic terminals, which cover 85% of the surface. In contrast, multipolar cell bodies are almost entirely wrapped by thin glial sheets—synaptic terminals contact less than 15% of the surface and tend to cluster at the bases of dendrites. Synaptic terminals are of three kinds, types 1, 2, and 3, which contain large round, small round-to-oval, and small flattened synaptic vesicles, respectively. Terminals of all three kinds synapse on both types of cell bodies. However, only globular cell bodies receive the largest type 1 terminals, which correspond to end-bulbs, seen in Golgi impregnations to arise from cochlear nerve axons. Cochlear ablation leads to degeneration of type 1, but not type 2 or 3 terminals.We conclude that neurons with globular cell bodies receive heavy somatic input from the cochlear nerve, as well as from other sources. Neurons with multipolar cell bodies receive very little input to their perikarya—giving their dendrites a more important role in determining their response properties. We suggest a morphological basis for correlating individual kinds of neurons with certain electrophysiological response types.     

Inferior colliculus in the rat: neuronal responses to stimulation of the auditory cortex

Responses to electrical stimulation of the auditory cortex (silver ball bipolar electrodes, single pulses, duration 0.2 ms, current 0.1-1.5 mA) were recorded in neurones in the inferior colliculus of rats anaesthetized with pentobarbital. Excitatory or inhibitory effects were obtained in 84 out of 162 recorded neurones. The majority of neurones responded with a short excitatory burst (with a latency from 3 to 15 ms); in some of them the initial excitation was followed by inhibition lasting from 30 to 150 ms. Few neurones only reacted to electrical stimulation by inhibition, which occurred 3-10 ms after the stimulus and lasted up to 300 ms. The inhibition either suppressed the spontaneous activity or the acoustically evoked response. Neurones reacting to stimulation of the auditory cortex were found mainly in the caudal and dorsal parts of the inferior colliculus.     

The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Golgi and Nissl methods

This report characterizes the cells and fibers in one part of the cochlear nucleus, the posterior division of the anteroventral cochlear nucleus. This includes the region where the cochlear nerve root enters the brain and begins to form endings. Nissl stains reveal the somata of globular cells with dispersed Nissl substance and those of multipolar cells with coarse, clumped Nissl bodies. Both parts of the posterior division contain cells with each Nissl pattern, but in different relative numbers and locations. Golgi impregnations demonstrate two types of neurons: bushy cells, with short bush-like dendrites, and stellate and elongate cells, with long tapered dendrites. Several varieties of bushy cells, differing in the morphology of the cell body and in the size and extent of the dendritic field, can be distinguished. Comparison of the distributions of these cell types, as well as cellular morphology, suggest that the globular cells recognized in Nissl stains correspond to bushy neurons, while the multipolar cells correspond to stellate and elongate neurons. Golgi impregnations reveal large end-bulbs and smaller boutons from cochlear nerve fibers, as well as boutons from other, unidentified sources, ending in this region.The particular arrangements of the dendritic fields of the different cell types and the axonal endings associated with them indicate that these neurons must have different physiological properties, since they define different domains with respect to the cochlear and non-cochlear inputs.     

Electrical stimulation of arterial and central chemosensory afferents at different times in the respiratory cycle of the cat: I. Ventilatory responses

Ventilatory responses to stimulation of chemoreceptor afferents were studied in the anesthetized, spontaneously breathing cat. Short bursts of electrical stimuli were applied, at various times in the inspiratory or expiratory phase of consecutive breaths, to the carotid sinus (CSN) and aortic nerves (AN) and to the ventral medulla (VM), and effects on tidal volume (V _T), inspiratory, expiratory and cycle durationst _I,t _E,t _tot) and in ventilation (_E) were measured. The responses evoked by stimulating CSN, AN and VM were qualitatively the same, although there were quantitative differences. It was found that effects of stimulation in expiration were restricted to the expiratory phase, and vice versa for inspiration. Stimulation during both inspiration and expiration resulted in increasedV _T, by increasing end-inspiratory or decreasing end-expiratory lung volume, respectively, and also increased ventilation, _E. These effects were most marked in response to stimulation in inspiration. During both phases there was an increasing effect with increasing delay of the stimulus,t _St, from onset of inspiration or expiration, respectively. There was a continuous increase int _I, from below control to above control values, with increasingt _St during inspiration and similarly fort _E during expiration. Hence, the total respiratory cycle duration was shortened when a stimulus was applied early in either phase, and was prolonged, when it was applied late. The results show that stimulation of peripheral and of central chemoafferents exerts qualitatively similar effects on respiration. The central neuronal mechanisms generating both inspiration and expiration show the same changes in reactivity in the respiratory cycle.Supported by the Deutsche Forschungsgemeinschaft, SFB 114 Bionach     

Perceptual learning: psychophysical thresholds and electrical brain topography.

We studied perceptual learning by determining psychophysical discrimination thresholds for visual hyper acuity targets (vernier stimuli) as a function of stimulus orientation. One aim was to relate perceptual improvements to changes of electrophysiological activity of the human brain. A group of 43 healthy adults participated in a psychophysical experiment where vernier thresholds for vertical and horizontal vernier targets were compared. In 16 subjects thresholds were measured for each orientation twice at an interval of 25 min. Between threshold estimations, evoked brain activity was recorded from 30 electrodes over the occipital brain areas while the subjects observed appearance and disappearance of supra-threshold vernier offsets. Mean evoked potentials were computed for the first and second 600 stimulus presentations, and the scalp topography of electrical brain activity was analyzed. Vertically oriented stimuli yielded significantly better performance than horizontal targets, and thresholds were significantly lower in the second half of the experiment, i.e. after prolonged viewing of stimuli. The improvements in discrimination performance were specific for stimulus orientation and did not generalize. Learning effects were also observed with electrical brain activity, and field strength of the potentials increased significantly as a function of time. Scalp topography of the evoked components was significantly affected indicating a shift of activation between different neuronal elements induced by perceptual learning.