Dexter R. F. Irvine

Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I : Effects of variation of stimulus parameters

In the primary auditory cortex (AI) of barbiturate-anesthetized cats multi-unit responses to tones and to frequency-modulated (FM) tonal stimuli were analyzed. Characteristic frequency (CF), sharpness of tuning, minimum threshold, and dynamic range of spike count--intensity functions were determined. Minimum threshold and dynamic range were positively correlated. The response functions to unidirectional FM sweeps of varying linear rate of change of frequency (RCF) that traversed the excitatory frequency response areas (FRAs) displayed a variety of shapes. Preferences for fast RCFs (> 1000 kHz/s) were most common. Best RCF was not correlated with measures of sharpness of tuning. Directional preference and sensitivity were quantified by a DS index which varied with RCF. About two-thirds of the multi-unit responses showed a preference for downward sweeps. Directional sensitivity was independent of CF and independent of best RCF. Measurements of latencies of phasic responses to unidirectional FM sweeps of different RCF demonstrated that the discharges of a given multi-unit over its effective RCF range were initiated at the same instantaneous frequency (effective Fi), independent of RCF. Effective Fis fell within the excitatory FRA of a given multi-unit. The relationships of effective Fis to CF show that responses were evoked only when the frequency of the signal was modulated towards CF and not when modulated away from it, and that responses were initiated before the modulation reached CF. Changes in the range and depth of modulation had only minor, if any, effects on RCF response characteristics, FM directional sensitivity, and effective Fis, as long as the beginning and ending frequencies of FM sweeps fell outside a multi-units FRA. Stimulus intensity also had only moderate effects on RCF response characteristics and DS. However, effective Fis were influenced in systematic fashions; with increases in intensity, effective Fis to upward and downward sweeps decreased and increased, respectively. Thus, for higher intensities FM responses were initiated at instantaneous frequencies occurring earlier in the signal. The results are compared with previous data on tone and FM sensitivity of auditory neurons in cortical and subcortical structures, and mechanisms of FM rate and directional sensitivity are discussed. The topographic representations of these neuronal properties in AI are reported in the companion report.

Cochlear Implants and Brain Plasticity

Cochlear implants have been implanted in over 110,000 deaf adults and children worldwide and provide these patients with important auditory cues necessary for auditory awareness and speech perception via electrical stimulation of the auditory nerve (AN). In 1942, Woolsey and Walzl presented the first report of cortical responses to localised electrical stimulation of different sectors of the AN in normal hearing cats, and established the cochleotopic organization of the projections to primary auditory cortex. Subsequently, individual cortical neurons in normal hearing animals have been shown to have well characterized input-output functions for electrical stimulation and decreasing response latencies with increasing stimulus strength. However, the central auditory system is not immutable, and has a remarkable capacity for plastic change, even into adulthood, as a result of changes in afferent input. This capacity for change is likely to contribute to the ongoing clinical improvements observed in speech perception for cochlear implant users. This review examines the evidence for changes of the response properties of neurons in, and consequently the functional organization of, the central auditory system produced by chronic, behaviourally relevant, electrical stimulation of the AN in profoundly deaf humans and animals.

Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage.

The adult auditory cortex is capable of a plastic reorganization of its tonotopic map after damage to restricted parts of the cochlear sensory epithelium. We examine the precise conditions of cochlear damage required to demonstrate such plasticity in the primary auditory cortex (A1) of the cat and the changes observed in neuronal responses in the A1 which has reorganized in plasticity of the tonotopic map. From these data we attempt to predict the conditions required for similar plasticity to occur in humans after coachlear damage.

Properties of single neurons in the anterior auditory field (AAF) of cat cerebral cortex

Abstract In the cortex of 6 anesthetized cats, the anterior auditory field (AAF) was defined by microelectrode maps of its frequency organization, and the responses to monaural and binaural tonal stimuli of single neurons in that field were examined qunatitatively. AAF neurons were sharply tuned to tonal frequency, had intensity dynamic ranges of less than 30–40 dB at best frequency, and had minimum response latencies generally in the order of 10–15 ms. The binaural interactions of AAF neurons were qualitatively similar to those of AI cells, with the possible exception of a relatively greater proportion of AAF neurons receiving stronger excitatory input from the ipsilateral ear. On the basis of these data and recent anatomical evidence, the proposal that AAF and AI function as parallel processors of ascending acoustic information is discussed.

Loudness perception and frequency discrimination in subjects with steeply sloping hearing loss: Possible correlates of neural plasticity

Loudness functions and frequency difference limens (DLFs) were measured in five subjects with steeply sloping high-frequency sensorineural hearing loss. The stimuli were pulsed pure tones encompassing a range of frequencies. Loudness data were obtained using a 2AFC matching procedure with a 500-Hz reference presented at a number of levels. DLFs were measured using a 3AFC procedure with intensities randomized within 6 dB around an equal-loudness level. Results showed significantly shallower loudness functions near the cutoff frequency of the loss than at a lower frequency, where hearing thresholds were near normal. DLFs were elevated, on average, relative to DLFs measured using the same procedure in five normally hearing subjects, but showed a local reduction near the cutoff frequency in most subjects with high-frequency loss. The loudness data are generally consistent with recent models that describe loudness perception in terms of peripheral excitation patterns that are presumably restricted by a steeply sloping hearing loss. However, the DLF data are interpreted with reference to animal experiments that have shown reorganization in the auditory cortex following the introduction of restricted cochlear lesions. Such reorganization results in an increase in the spatial representation of lesion-edge frequencies, and is comparable with the functional reorganization observed in animals following frequency-discrimination training. It is suggested that similar effects may occur in humans with steeply sloping high-frequency hearing loss, and therefore, the local reduction in DLFs in our data may reflect neural plasticity.

Auditory response properties of neurons in the anterior ectosylvian sulcus of the cat

The auditory response properties of single neurons in the fundus and banks of the anterior ectosylvian sulcus (AES) were studied with simple dichotic stimuli (viz. noise- and tone-bursts) in cats anaesthetized with alpha-chloralose. Neurons within AES showed simple onset responses, were most commonly excited by stimulation of both ears, and showed either broad tuning or multiple high best frequencies. Some neurons were also tested for visual responsiveness and it was found that auditory cells and visual cells were intermingled within the sulcus. A small percentage of cells responded to both auditory and visual stimulation. Overall, the response properties of AES neurons differed from those of nearby auditory cortical fields. The region of AES studied appears to be outside the recently defined fourth somatosensory area (SIV), but overlaps para-SIV found deeper in the sulcus. It appears that deep within the sulcus and along most of its length there is a population of auditory, somatosensory and visual cells; to delineate this auditory population from the surrounding auditory cortical fields this region has been designated Field AES.

Rapid changes in the frequency tuning of neurons in cat auditory cortex resulting from pure-tone-induced temporary threshold shift.

The response areas (frequency by intensity) of single neurons in primary auditory cortex of anesthetized cats were studied before and after temporary threshold shifts in cochlear sensitivity induced by an intense pure tone. Cochlear temporary threshold shift was monitored through the threshold of the gross auditory nerve compound action potential and in most cases involved a notch-like loss centered at the characteristic frequency of the unit under study. Only two neurons showed changes in response area that mirrored the changes at the auditory periphery. Most neurons (14) showed more complex changes involving both expansion and contraction of response areas. Expansion of response areas was indicated by lower thresholds at some frequencies and by the emergence of sensitivity to previously ineffective frequencies. A change was classified as contraction when the response area after the intense-tone exposure was smaller than would be expected by applying the profile of the temporary threshold shift to the initial response area. Contraction of both upper (high intensity) and lower boundaries of response areas was found; in the most extreme cases, neurons were totally unresponsive after the intense-tone exposure. The complexity of effects of temporary threshold shifts on the response areas of cortical neurons is likely to be related to mechanisms that normally determine the frequency response limits of these neurons. The response areas of cortical neurons are more complex than those of auditory nerve fibers, and are thought to reflect the integration of excitatory and inhibitory inputs. The variety of effects observed in this study are consistent with the excitatory and inhibitory components of the response area of a given neuron being differentially affected by the temporary threshold shift.

Specificity of perceptual learning in a frequency discrimination task

On a variety of visual tasks, improvement in perceptual discrimination with practice (perceptual learning) has been found to be specific to features of the training stimulus, including retinal location. This specificity has been interpreted as evidence that the learning reflects changes in neuronal tuning at relatively early processing stages. The aim of the present study was to examine the frequency specificity of human auditory perceptual learning in a frequency discrimination task. Difference limens for frequency (DLFs) were determined at 5 and 8 kHz, using a three-alternative forced choice method, for two groups of eight subjects before and after extensive training at one or the other frequency. Both groups showed substantial improvement at the training frequency, and much of this improvement generalized to the nontrained frequency. However, a small but statistically significant component of the improvement was specific to the training frequency. Whether this specificity reflects changes in neural frequency tuning or attentional changes remains unclear.

Cochlear implant use following neonatal deafness influences the cochleotopic organization of the primary auditory cortex in cats

Electrical stimulation of spiral ganglion neurons in a deafened cochlea, via a cochlear implant, provides a means of investigating the effects of the removal and subsequent restoration of afferent input on the functional organization of the primary auditory cortex (AI). We neonatally deafened 17 cats before the onset of hearing, thereby abolishing virtually all afferent input from the auditory periphery. In seven animals the auditory pathway was chronically reactivated with environmentally derived electrical stimuli presented via a multichannel intracochlear electrode array implanted at 8 weeks of age. Electrical stimulation was provided by a clinical cochlear implant that was used continuously for periods of up to 7 months. In 10 long‐term deafened cats and three age‐matched normal‐hearing controls, an intracochlear electrode array was implanted immediately prior to cortical recording. We recorded from a total of 812 single unit and multiunit clusters in AI of all cats as adults using a combination of single tungsten and multichannel silicon electrode arrays. The absence of afferent activity in the long‐term deafened animals had little effect on the basic response properties of AI neurons but resulted in complete loss of the normal cochleotopic organization of AI. This effect was almost completely reversed by chronic reactivation of the auditory pathway via the cochlear implant. We hypothesize that maintenance or reestablishment of a cochleotopically organized AI by activation of a restricted sector of the cochlea, as demonstrated in the present study, contributes to the remarkable clinical performance observed among human patients implanted at a young age. J. Comp. Neurol. 512:101–114, 2009.

The development of some peripheral and central auditory responses in the neonatal cat

The development of cochlear nerve action potential thresholds at different frequencies (AP audiograms) and inferior colliculus (IC) single unit thresholds and tuning was examined in barbiturate-anaesthetized kittens. AP thresholds decreased over the whole frequency spectrum during the first 5 weeks of life. Thresholds to high-frequency stimulation remained higher in 7-week-old animals than in adults. These results are in contrast to previous reports which have suggested that the AP response and gross cochlear anatomy are mature by the end of the second week. These differences may be due to the fact that the AP audiogram technique provides a measure of the activity of discrete regions along the cochlear partition. IC units in animals younger than 3.5 weeks had significantly elevated thresholds and broader tuning than those of the adult cat. Comparison of AP audiogram and IC unit thresholds in the adult revealed that these indices show similar frequency-dependent sensitivity. The slower maturation revealed by the AP audiogram may be due to the greater number and/or synchrony of cochlear nerve discharges needed to produce the gross AP. If this were the case, perception of suprathreshold sounds might not develop as quickly as thresholds for sound detection.