scholarly journals The Role of Adaptation in Generating Monotonic Rate Codes in Auditory Cortex

2019 ◽  
Author(s):  
Jong Hoon Lee ◽  
Xiaoqin Wang ◽  
Daniel Bendor

AbstractIn primary auditory cortex, slowly repeated acoustic events are represented temporally by phase-locked activity of single neurons. Single-unit studies in awake marmosets (Callithrix jacchus) have shown that a sub-population of these neurons also monotonically increase or decrease their average discharge rate during stimulus presentation for higher repetition rates. Building on a computational single-neuron model that generates phase-locked responses with stimulus evoked excitation followed by strong inhibition, we find that stimulus-evoked short-term depression is sufficient to produce synchronized monotonic positive and negative responses to slowly repeated stimuli. By exploring model robustness and comparing it to other models for adaptation to such stimuli, we conclude that short-term depression best explains our observations in single-unit recordings in awake marmosets. Using this model, we emulated how single neurons could encode and decode multiple aspects of an acoustic stimuli with the monotonic positive and negative encoding of a given stimulus feature. Together, our results show that a simple biophysical mechanism in single neurons can allow a more complex encoding and decoding of acoustic stimuli.

1995 ◽  
Vol 74 (5) ◽  
pp. 1841-1855 ◽  
Author(s):  
D. M. Bowman ◽  
J. J. Eggermont ◽  
G. M. Smith

1. Neural activity was recorded extracellularly with two independent microelectrodes aligned in parallel and advanced perpendicular to isofrequency sheets in cat primary auditory cortex. Multiunit activity was separated into single-unit spike trains using a maximum variance spike sorting algorithm. Only units that demonstrated a high quality of sorting and a minimum spontaneous firing rate of 0.2 spikes/s were considered for analysis. The primary aim of this study was to describe the effect of periodic click train and broadband noise stimulation on short-time-scale (< or = 50 ms) bursts in the spike trains of single auditory cortical units and to determine whether stimulation influenced the occurrence, spike count, and/or temporal structure of burst firing relative to a spontaneous baseline. 2. Extracellular recordings were made in 20 juvenile and adult cats from 69 single auditory cortical units during click train stimulation and silence, and from 30 single units during noise stimulation and in silence. In an additional 15 single units the effect of both click train and noise stimulation was investigated. The incidence, spike count, and temporal structure of short-time-scale burst firing in the first 100 ms following stimulus presentation was compared with burst firing in the period starting 500 ms after stimulus presentation and with spontaneous burst firing. In addition, the serial dependence of interspike intervals within a burst was tested during periods of stimulation. 3. Burst firing was present in the stimulation, poststimulation, and spontaneous conditions. Longer bursts (consisting of > or = 3 spikes) were more commonly observed in the poststimulation and spontaneous conditions than in the stimulation condition. This effect was most pronounced during click stimulation. A period of elevated firing activity was present in a subset of units 0.5-1.5 s after stimulus presentation, indicating prolonged effects of stimulation on single-unit firing behavior. 4. For both stimuli, the proportion of single-unit responses composed of bursts was significantly greater in poststimulation and spontaneous periods than during stimulation. Burst rate was higher in post-click-train stimulation and spontaneous periods than during periods of click stimulation. The isolated spike rate was significantly higher during periods of noise and click stimulation than in the poststimulation and spontaneous periods. 5. An examination of the autocorrelograms and higher-order interspike interval histograms of single-unit responses during click train stimulation indicated that 25% of single-unit spike trains contained an excess of brief first-order intervals and 14% of spike trains contained a shortage of long higher-order interspike intervals relative to a spontaneous baseline. During noise stimulation, 10% of single-unit responses contained an excess of short intervals relative to baseline. Interspike intervals of short-duration bursts were not serially dependent during periods of stimulation. 6. A comparison of the autocorrelograms and higher-order interval histograms of single-unit responses in the poststimulation and spontaneous conditions indicated that 20% of single-unit spike trains contained an excess of short first-, second-, and third-order intervals following stimulation. This subgroups of single units could not be distinguished on the basis of the age of the animal or the depth at which the recording was made. 7. The low incidence of burst firing during stimulation opposes the view that bursts serve as a mechanism to emphasize or amplify particular stimulus-related responses in the presence of ongoing spontaneous activity in the primary auditory cortex. Moreover, there is little evidence to support the notion that brief bursts represent neural codes, because intraburst intervals are not serially dependent. It is suggested that pyramidal burst firing may be an effective way to evoke postsynaptic firing in inhibitory interneurons and subsequ


2001 ◽  
Vol 85 (6) ◽  
pp. 2350-2358 ◽  
Author(s):  
Sanjiv K. Talwar ◽  
Pawel G. Musial ◽  
George L. Gerstein

Studies in several mammalian species have demonstrated that bilateral ablations of the auditory cortex have little effect on simple sound intensity and frequency-based behaviors. In the rat, for example, early experiments have shown that auditory ablations result in virtually no effect on the rat's ability to either detect tones or discriminate frequencies. Such lesion experiments, however, typically examine an animal's performance some time after recovery from ablation surgery. As such, they demonstrate that the cortex is not essential for simple auditory behaviors in the long run. Our study further explores the role of cortex in basic auditory perception by examining whether the cortex is normally involved in these behaviors. In these experiments we reversibly inactivated the rat primary auditory cortex (AI) using the GABA agonist muscimol, while the animals performed a simple auditory task. At the same time we monitored the rat's auditory activity by recording auditory evoked potentials (AEP) from the cortical surface. In contrast to lesion studies, the rapid time course of these experimental conditions preclude reorganization of the auditory system that might otherwise compensate for the loss of cortical processing. Soon after bilateral muscimol application to their AI region, our rats exhibited an acute and profound inability to detect tones. After a few hours this state was followed by a gradual recovery of normal hearing, first of tone detection and, much later, of the ability to discriminate frequencies. Surface muscimol application, at the same time, drastically altered the normal rat AEP. Some of the normal AEP components vanished nearly instantaneously to unveil an underlying waveform, whose size was related to the severity of accompanying behavioral deficits. These results strongly suggest that the cortex is directly involved in basic acoustic processing. Along with observations from accompanying multiunit experiments that related the AEP to AI neuronal activity, our results suggest that a critical amount of activity in the auditory cortex is necessary for normal hearing. It is likely that the involvement of the cortex in simple auditory perceptions has hitherto not been clearly understood because of underlying recovery processes that, in the long-term, safeguard fundamental auditory abilities after cortical injury.


2005 ◽  
Vol 94 (4) ◽  
pp. 2263-2274 ◽  
Author(s):  
Jiping Zhang ◽  
Kyle T. Nakamoto ◽  
Leonard M. Kitzes

Sounds commonly occur in sequences, such as in speech. It is therefore important to understand how the occurrence of one sound affects the response to a subsequent sound. We approached this question by determining how a conditioning stimulus alters the response areas of single neurons in the primary auditory cortex (AI) of barbiturate-anesthetized cats. The response areas consisted of responses to stimuli that varied in level at the two ears and delivered at the characteristic frequency of each cell. A binaural conditioning stimulus was then presented ≥50 ms before each of the stimuli comprising the level response area. An effective preceding stimulus alters the shape and severely reduces the size and response magnitude of the level response area. This ability of the preceding stimulus depends on its proximity in the level domain to the level response area, not on its absolute level or on the size of the response it evokes. Preceding stimuli evoke a nonlinear inhibition across the level response area that results in an increased selectivity of a cortical neuron for its preferred binaural stimuli. The selectivity of AI neurons during the processing of a stream of acoustic stimuli is likely to be restricted to a portion of their level response areas apparent in the tone-alone condition. Thus rather than being static, level response areas are fluid; they can vary greatly in extent, shape and response magnitude. The dynamic modulation of the level response area and level selectivity of AI neurons might be related to several tasks confronting the central auditory system.


1999 ◽  
Vol 82 (6) ◽  
pp. 3506-3526 ◽  
Author(s):  
Marcia W. Raggio ◽  
Christoph E. Schreiner

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.


1993 ◽  
Vol 70 (2) ◽  
pp. 492-511 ◽  
Author(s):  
F. K. Samson ◽  
J. C. Clarey ◽  
P. Barone ◽  
T. J. Imig

1. Single-unit recordings were carried out in primary auditory cortex (AI) of barbiturate-anesthetized cats. Neurons, sensitive to sound direction in the horizontal plane (azimuth), were identified by their responses to noise bursts, presented in the free field, that varied in azimuth and sound pressure level (SPL). SPLs typically varied between 0 and 80 dB and were presented at each azimuth that was tested. Each azimuth-sensitive neuron responded well to some SPLs at certain azimuths and did not respond well to any SPL at other azimuths. This report describes AI neurons that were sensitive to the azimuth of monaurally presented noise bursts. 2. Unilateral ear plugging was used to test each azimuth-sensitive neuron's response to monaural stimulation. Ear plugs, produced by injecting a plastic ear mold compound into the concha and ear canal, attenuated sound reaching the tympanic membrane by 25-70 dB. Binaural interactions were inferred by comparing responses obtained under binaural (no plug) and monaural (ear plug) conditions. 3. Of the total sample of 131 azimuth-sensitive cells whose responses to ear plugging were studied, 27 were sensitive to the azimuth of monaurally presented noise bursts. We refer to these as monaural directional (MD) cells, and this report describes their properties. The remainder of the sample consisted of cells that either required binaural stimulation for azimuth sensitivity (63/131), because they were insensitive to azimuth under unilateral ear plug conditions or responded too unreliably to permit detailed conclusions regarding the effect of ear plugging (41/131). 4. Most (25/27) MD cells received either monaural input (MD-E0) or binaural excitatory/inhibitory input (MD-EI), as inferred from ear plugging. Two MD cells showed other characteristics. The contralateral ear was excitatory for 25/27 MD cells. 5. MD-E0 cells (22%, 6/27) were monaural. They were unaffected by unilateral ear plugging, showing that they received excitatory input from one ear, and that stimulation of the other ear was without apparent effect. On the other hand, some monaural cells in AI were insensitive to the azimuth of noise bursts, showing that sensitivity to monaural directional cues is not a property of all monaural cells in AI. 6. MD-EI cells (70%, 19/27) exhibited an increase in responsiveness on the side of the plugged ear, showing that they received excitatory drive from one ear and inhibitory drive from the other. MD-EI cells remained azimuth sensitive with the inhibitory ear plugged, showing that they were sensitive to monaural directional cues at the excitatory ear.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 56 (3) ◽  
pp. 663-682 ◽  
Author(s):  
R. A. Reale ◽  
R. E. Kettner

Responses from neuron clusters were used to derive binaural and aural dominance maps within the 5- to 30-kHz frequency representation of the primary auditory cortical (AI) field in the barbiturate-anesthetized cat. Tone burst stimuli were presented dichotically using a calibrated and sealed acoustic delivery system to parametrically vary interaural intensity difference (IID). Neuron cluster responses were divided into three binaural interaction classes using audiovisual criteria: summation (56%), suppression (25%), and mixed (17%). Neurons in the summation and suppression classes demonstrated a single type of binaural interaction, regardless of intensity manipulations. Neurons in the mixed binaural class demonstrated summation responses when dichotic tonal intensities were near their threshold levels and the IID was small, but suppression responses when the IID was increased. The relative proportions of the three binaural interaction classes changed with distance along the dorsal-to-ventral isofrequency dimension. Nearly equal proportions of each class were observed at the ventral end of field AI, whereas quite different proportions of each class were seen at the dorsal extreme of the field. The average frequency of occurrence of the mixed binaural class increased nearly monotonically with increasing distance from the dorsal end of field AI. The majority of mapped AI loci exhibited a contralateral aural dominance (65%) with equidominance (25%), ipsilateral aural dominance (6%), and predominantly binaural (4%) classes accounting for the remainder. Average topographic distributions of aural dominance suggested that the ventral end of field AI consisted almost exclusively of the contralateral dominance class, whereas more equal proportions of the four classes were observed near the dorsal extreme of the field. The highest average proportions of ipsilateral aural dominance and predominantly binaural classes were found in the dorsal half of field AI. Single neurons, isolated at cortical loci assigned to the mixed binaural class during the mapping of neuron clusters, were shown to demonstrate both summation and suppression responses. Quantitative measurements relating either discharge rate or response latency to changes in the IID appeared to distinguish these cells from other single neurons studied. Typically, the probability of discharge was initially increased and subsequently decreased by progressive changes in IID that increased the intensity of the ipsilateral tone relative to the contralateral tone. The initial changes in IID characteristically shortened the latent period to the binaural response while subsequent increments in IID produced a more comp


2003 ◽  
Vol 89 (6) ◽  
pp. 3190-3204 ◽  
Author(s):  
Marcia W. Raggio ◽  
Christoph E. Schreiner

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.


2014 ◽  
Vol 2014 ◽  
pp. 1-11 ◽  
Author(s):  
Iiro P. Jääskeläinen ◽  
Jyrki Ahveninen

The ability to concentrate on relevant sounds in the acoustic environment is crucial for everyday function and communication. Converging lines of evidence suggests that transient functional changes in auditory-cortex neurons, “short-term plasticity”, might explain this fundamental function. Under conditions of strongly focused attention, enhanced processing of attended sounds can take place at very early latencies (~50 ms from sound onset) in primary auditory cortex and possibly even at earlier latencies in subcortical structures. More robust selective-attention short-term plasticity is manifested as modulation of responses peaking at ~100 ms from sound onset in functionally specialized nonprimary auditory-cortical areas by way of stimulus-specific reshaping of neuronal receptive fields that supports filtering of selectively attended sound features from task-irrelevant ones. Such effects have been shown to take effect in ~seconds following shifting of attentional focus. There are findings suggesting that the reshaping of neuronal receptive fields is even stronger at longer auditory-cortex response latencies (~300 ms from sound onset). These longer-latency short-term plasticity effects seem to build up more gradually, within tens of seconds after shifting the focus of attention. Importantly, some of the auditory-cortical short-term plasticity effects observed during selective attention predict enhancements in behaviorally measured sound discrimination performance.


1998 ◽  
Vol 7 (2) ◽  
pp. 99-109 ◽  
Author(s):  
Naohito Fujiwara ◽  
Takashi Nagamine ◽  
Makoto Imai ◽  
Tomohiro Tanaka ◽  
Hiroshi Shibasaki

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