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W. M. Keck Center for Integrative Neuroscience, University of California at San Francisco, San Francisco, California 94143-0732
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Brosch, Michael and Christoph E. Schreiner. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77: 923-943, 1997. Nonsimultaneous two-tone interactions were studied in the primary auditory cortex of anesthetized cats. Poststimulatory effects of pure tone bursts (masker) on the evoked activity of a fixed tone burst (probe) were investigated. The temporal interval from masker onset to probe onset (stimulus onset asynchrony), masker frequency, and intensity were parametrically varied. For all of the 53 single units and 58 multiple-unit clusters, the neural activity of the probe signal was either inhibited, facilitated, and/or delayed by a limited set of masker stimuli. The stimulus range from which forward inhibition of the probe was induced typically was centered at and had approximately the size of the neuron's excitatory receptive field. This "masking tuning curve" was usually V shaped, i.e., the frequency range of inhibiting masker stimuli increased with the masker intensity. Forward inhibition was induced at the shortest stimulus onset asynchrony between masker and probe. With longer stimulus onset asynchronies, the frequency range of inhibiting maskers gradually became smaller. Recovery from forward inhibition occurred first at the lower- and higher-frequency borders of the masking tuning curve and lasted the longest for frequencies close to the neuron's characteristic frequency. The maximal duration of forward inhibition was measured as the longest period over which reduction of probe responses was observed. It was in the range of 53-430 ms, with an average of 143 ± 71 (SD) ms. Amount, duration and type of forward inhibition were weakly but significantly correlated with "static" neural receptive field properties like characteristic frequency, bandwidth, and latency. For the majority of neurons, the minimal inhibitory masker intensity increased when the stimulus onset asynchrony became longer. In most cases the highest masker intensities induced the longest forward inhibition. A significant number of neurons, however, exhibited longest periods of inhibition after maskers of intermediate intensity. The results show that the ability of cortical cells to respond with an excitatory activity depends on the temporal stimulus context. Neurons can follow higher repetition rates of stimulus sequences when successive stimuli differ in their spectral content. The differential sensitivity to temporal sound sequences within the receptive field of cortical cells as well as across different cells could contribute to the neural processing of temporally structured stimuli like speech and animal vocalizations.
Many natural sounds and communication sounds consist of temporal sequences of spectrally complex acoustic events. In speech, important information-carrying temporal features are the duration, separation, and order of individual segments. Depending on their spectral composition, duration, and temporal separation, successive auditory events may be perceived as a single auditory stream or are segregated into different auditory streams (Bregman 1990 Surgery
A total of 12 experiments was conducted on adult cats. The methods for surgical preparation, recording, and stimulation techniques were similar to those described previously (Schreiner and Mendelson 1990 Neural recording
One or two closely spaced tungsten microelectrodes (1-2 M Acoustic stimulation
Experiments were performed in a double-walled sound-shielded chamber (IAC). Acoustic stimuli were generated by a microcomputer (TMS 32010 or TMS 320C30) at a sampling rate of 8 or 16 µs with a dynamic range of 80 dB. The signal was fed into an antialiasing filter (55 kHz; 96 dB/octave). Additional attenuation was provided by two passive attenuators (Hewlett-Packard or Tucker Davis, PA4). The attenuated signal was amplified and delivered via headphones (STAX 54) to both ears. Depending on the type of binaural interaction of the neuron under investigation, stimuli were presented to the contralateral ear, to the ipsilateral ear, or to both ears.
Data analysis
For each frequency-intensity combination of the variable tone, the number of neural discharges during the presentation of the first (and the 2nd) stimulus were plotted in two-dimensional boxes to obtain stimulus response areas (e.g., Fig. 2). If receptive fields were determined, the response during the presentation of the variable tone was analyzed. If the time course of two-tone interactions was determined, the response during the presentation of the probe was analyzed.
The results of this study are presented in three parts. The first part illustrates with three examples how masker stimuli of different frequencies and intensities affect neural responsiveness following the presentation of the masker. Three types of influence of a masker on the neural excitability are described. The second part reports general properties of the influence of different maskers and relates the temporal characteristics of neurons to their static receptive field properties. The presentation is concluded by briefly demonstrating the effects of two-tone interactions with stimulus pairs of different duration.
Examples of MTCs
Figure 3 gives an example of the temporal course of two-tone interactions in AI. Temporal interactions were tested with 675 different masker conditions and six different SOAs of a fixed probe signal. The first stimulus of each pair (masker) varied in frequency and intensity, whereas the second stimulus (probe) was a constant 880-Hz tone burst at an intensity of 63 dB SPL. In this and the following figures, raw data are displayed without additional low-pass filtering. The first frame shows for each frequency-intensity combination of the masker the number of neural discharges registered during the presentation of the masker. The length of the bars indicates the number of action potentials. Thus this plot shows the extent of the excitatory regions of the receptive field of the neuron. The other frames display the responses to the second stimulus of each pair, which was always constant in frequency and intensity. The response strength of the fixed stimulus is plotted at the location of each masker condition in the frequency-intensity plane. The resulting patterns reflect the interaction of the masker stimulus with the response of the probe. They show that neural response to the second stimulus depended on the frequency and intensity of the first stimulus. When the probe was presented immediately after the cessation of the masker (2nd frame), the neuron did not respond to the probe for a wide range of masker frequency-intensity combinations. Such inhibition of probe responses was mostly seen when the neuron had already responded to the masker itself, i.e., when the masker was within the excitatory receptive field. When the masker was well outside the receptive field of the neuron, proberesponses were unaffected. Masker conditions near but outside the border of the excitatory receptive field also often inhibited the probe stimulus. This forward inhibition of neural activity lasted for up to several hundred milliseconds. The following frames demonstrate that the range of inhibiting maskers became gradually smaller as the temporal separation of masker and probe onsets was extended. Recovery from forward inhibition of the CF probe tone is first accomplished for maskers at the low- and high-frequency borders of the receptive field and for low-intensity maskers. Forward inhibition lasted the longest for masker frequencies at the center of the excitatory receptive field, i.e., around the neuron's CF.
Quantitative description of the time course of forward inhibition
For a quantitative description of the spectrotemporal dependence of forward inhibition, several parameters of MTCs were obtained for each SOA (Fig. 2). The main parameters were the lowest and highest inhibitory masker frequencies 10 and 40 dB (in a few cases 35 dB) above minimum excitatory threshold, and the minimal and maximal intensities of the MTC that induced probe magnitude effects. Frequency values were expressed in octaves from the CF of the neuron. These values, together with the corresponding values of the excitatory receptive field, were plotted against the logarithm of SOA (Figs. 7 and 8).
General properties of forward inhibition
The properties of forward inhibition were obtained for a total of 53 single neurons and 58 multiunit clusters in AI. The CFs of the neurons were between 0.9 and 15.4 kHz (Fig. 12C). The ranges of latencies, thresholds (Fig. 12A), bandwidths (Fig. 12D), and nonmonotonicities were similar to those found in previous reports of the spatial distributions of these parameters in cats (e.g., Schreiner and Mendelson 1990
Comparison of MTC and receptive field for short SOAs
This and the following section compare spectrotemporal properties of forward inhibition and static receptive field properties. We first compared various receptive field parameters with corresponding parameters of MTCs at 30 ms, at which the most widespread forward inhibition was induced (Fig. 12). In general, MTCs were centered on and scaled to the receptive field of a neuron. Neurons with large receptive fields had large MTCs and vice versa. Minimal inhibitory masker intensity was slightly (6 dB for single units and 1 dB for multiunits) below the neural threshold. Differences were only significant for single units (Wilcoxon test, n = 43, Z = Relation of temporal characteristics of forward inhibition to static receptive properties
Several temporal characteristics of forward inhibition were compared with the static receptive field parameters by performing a correlation analysis (Table 1). Temporal characteristics included maximal duration of forward inhibition, decrease of frequency range of MTCs 40 dB above neural threshold, and change of the minimal and maximal inhibitory masker intensity between 30-ms SOA and three-fourths of the maximal duration of forward inhibition. For the latter parameter two groups were compared. The first group consisted of neurons in which forward inhibition was not induced from loud maskers at three fourths of the maximal duration of forward inhibition. In the second group no change of the maximal inhibitory masker intensity was observed. Static receptive field parameters included CF, bandwidth 40 dB above neural threshold (measured in octaves), neural threshold, turning point, nonmonotonicity of intensity-rate functions, and latency of first discharges.
Forward inhibition is affected by stimulus duration
The results presented so far were obtained with stimulus pairs of short duration (30 ms each for masker and probe tone). However, the properties of forward inhibition could depend on other parameters of the two tones as well. Specifically, the duration of the masker could have a strong influence on forward inhibition. Figure 13 shows an example for two-tone interactions tested with maskers of different duration. When the probe followed immediately after the cessation of a masker of short duration (30 ms), the neurons were inhibited from a broad range of maskers (Fig. 13B). The MTC was approximately of the size of the excitatory receptive field. For this cluster, forward inhibition lasted for 185 ms such that no effect of maskers on the neural activity was observed when probes were presented 190 ms after the onset of the masker (Fig. 13C). However, when the masker duration was prolonged to 190 ms and the effect on the neural activity was tested at the same SOA of 190 ms, inhibition of several probe responses was observed (Fig. 13D). Similar results were found in four other neurons (2 single units and 2 multiunits) where the masker duration was altered. This clearly demonstrates that forward inhibition reflects effects both from the onset of the masker and from the steady-state portion or offset of the masker.
This study addresses the question of spectrotemporal interaction in the cortical processing of stimulus sequences. Employing a very simple stimulus sequence of two pure tones, it was revealed that the responsiveness of neurons in the auditory cortex depends on the temporal stimulus context. Neural activity can be diminished or enhanced for a period of up to several hundred milliseconds because of the influence of a preceding stimulus. Duration of forward inhibition depended strongly on the frequency and intensity of the first tone of the stimulus pair, raising the question of whether spectral and temporal properties of cortical receptive fields can be described independently. Characteristics of forward inhibition were significantly but weakly linked with various static receptive field properties.
Determination of MTCs
MTCs were defined as the set of those maskers that inhibited the neural activity of the following probe tone. Inhibition of neural activity was assessed indirectly by presenting a probe tone at various intervals after the masker. If the response strength to the probe was significantly below its response strength if no masker was presented before the probe, a particular masker was inside the MTC. The uninfluenced probe response was estimated by measuring the average probe response strength after the presentation of maskers of very low intensity, under the assumption that a soft masker exerted only a marginal influence on the following neural activity. This value reflected the average probe response strength when probes were presented at the relatively slow repetition rate of the intertrial rate. In the current experiments the intertrial interval was between 350 and 1,030 ms. At these rates, the majority of cortical neurons responded slightly more weakly to the individual stimulus than if stimuli were presented in isolation. Hocherman and Gilat (1981) Effects of anesthesia
Most experiments were conducted under pentobarbital anesthesia. Pentobarbital is known to decrease the rate of spontaneous activity in the cortex. A reason for this effect may reside in the increase of the inhibitory postsynaptic potentials due to the enhanced sensitivity of Single-neuron versus multiple-neuron activity
The interpretation of the present study has to consider that recordings were made from both single neurons and from multiunit clusters. Multiunit activity reflects the action potentials generated by several neurons in the vicinity of the electrode tip. Because large cells have action potentials with greater amplitudes, extracellular single-unit recordings are most likely exclusively made from pyramidal cells, whereas other cell types such as stellate cells also contribute to multiunit recordings.
Generation of forward inhibition
Several mechanisms have to be considered regarding where and how forward inhibition/suppression of cortical neurons is generated. Nonneural causes such as suppressive effects of nonlinearities in basilar membrane motion, noninhibitory causes such as adaptation, and neural inhibitory effects accumulate and combine along the auditory pathway until they are revealed in the cortex by the forward masking technique applied in this study. Because most conditions in this study did not involve simultaneous presentation of masker and probe, instantaneous cochlear mechanic suppression effects did not contribute significantly to the observed effects.
Comparison with previous studies: inhibitory neural interactions
The capability of cortical neurons to process temporal aspects of stimuli has usually been assessed with double-pulse or periodically modulated stimuli. The latter have revealed modulation transfer functions that describe how a cell responds to different types of periodically modulated sounds, such as amplitude-modulated pure tones or noise, or click trains. Rate modulation transfer functions are related to the present results of forward masking, because both show how the discharge rate of neurons depends on the temporal interval between two acoustic transients. The comparison of the results obtained with the two paradigms, however, has to be taken into consideration as follows.
Comparison with previous studies: latency
The previous paragraphs discuss how the temporal stimulus context affects the discharge rate of cortical neurons. In addition to forward inhibition, the temporal stimulus context can also affect the latent period of neural discharges. Phillips et al. (1989) Relation of spectral and temporal properties of receptive fields
The previous discussion shows that neural responses to a sound depend on the temporal context within which the sound occurs. This implies that the set of stimuli that affects neural activity is not only dependent on the spectral composition of sounds but also on the temporal evolution of sounds. Receptive fields of auditory neurons thus extend both in the spectral and temporal domain. These two domains are not necessarily separable. A specific relation between the spectral and temporal aspects of the response characteristics of auditory neurons has been found for various cell types in the cochlear nucleus (reviewed in Langner 1992 Concluding remarks
Three concepts have traditionally been proposed for the neural encoding of acoustic information in the auditory system: the rate code, the temporal code, and the place code. In the present study we found that neural responses to the same stimulus were different if the stimulus occurred within a sequence of other stimuli compared with being presented in isolation. Thus the present study provides evidence that information about stimulus sequences may be coded in the auditory cortex by changes in the discharge rate (response strengths both decreased and increased), and by changes in the timing of neural responses. In addition, there were indications that neurons with different temporal response characteristics are located at different regions of AI.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). Numerous psychophysical studies have demonstrated that the temporal stimulus context affects the perceptual quality of individual auditory events. Detection thresholds of individual sounds can be elevated (Lüscher and Zwislocki 1947), and the subjective pitch and loudness (Stevens and Davis 1938) of auditory events can be altered by preceding and succeeding sounds. Although the perceptual consequences of the temporal stimulus context have been studied intensively, little information is available on the central neural mechanisms and neural structures underlying the processing of time-varying stimuli.
; Diamond et al. 1962; Kaas et al. 1967; Strominger et al. 1980) and tone durations (Scharlock et al. 1965). Lesions also result in permanent incapacities in discrimination of species-specific vocalizations in squirrel monkeys (Hupfer et al. 1977) and in macaques (Heffner and Heffner 1984), and induce aphasia-like deficits (Heffner and Heffner 1989).
; Eggermont 1991; Phillips et al. 1989; but see also de Ribaupierre et al. 1972). At higher repetition rates neurons typically only respond to the first element of the sequence but not at all or only weakly to the following elements. Similar results were obtained in studies with periodically modulated sounds (Eggermont 1994; Schreiner and Langner 1988; Schreiner and Urbas 1986, 1988). Neurons at subcortical stages of the auditory pathway, in contrast, generally respond to much higher repetition rates (e.g., Langner 1992). From these results it has been suggested that cortical neurons code for the time structure of transients of auditory signals, as first suggested by Creutzfeldt et al. (1980). There is anecdotal evidence that cells in auditory cortex might also serve as sequence detectors (McKenna et al. 1989; Riquimaroux 1994). Responses to individual pure tones could be enhanced or attenuated if they were succeeded by other tones within a period of several hundred milliseconds.
; Steinschneider et al. 1994; Wang et al. 1995; for review see Newman 1988). These studies utilized voice onset time continua, time-reversed vocalizations, and time-compressed or -expanded calls. Results indicate that the responses of cortical neurons depend on temporal features of communication sounds, such as the voice onset time and the temporal separation and temporal order of individual parts of calls.
). In that study, the authors concentrated on the explanation of potential origins of cortical forward masking, e.g., the relation to sideband inhibition and to nonmonotonic rate-level functions. In contrast, the focus of the present study was on the time course of two-tone interactions. The dependence of the duration of two-tone interactions on the frequency and intensity was quantitatively assessed. To attempt a description of the spectrotemporalresponse properties of auditory neurons, characteristics of two-tone interactions were then related to various "static" receptive field properties of the neurons, including characteristic frequency (CF), threshold, shape of rate-intensity functions, bandwidth, inhibitory subregions of the receptive field, and latent period of neural response. Recordings were performed both from single units and neural clusters, allowing an estimate of how characteristics of two-tone interactions are locally distributed. The present article describes the spectrotemporal characteristics of stimulus interactions for response inhibition and latency. The characteristics of forward facilitation will be described in a forthcoming article. Parts of the results have been published previously (Brosch and Schreiner 1994).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
), and were conducted according to the rules for animal experimentation of the American Society for Neuroscience. In brief, cats were initially anesthetized with a mixture of ketamine HCl (10 mg/kg) and acepromazine (0.28 mg/kg) given intramuscularly. An intravenous infusion line was placed and, for the following surgery, the cat received ~30 mg/kg Nembutal (titrated to effect). Body temperature was measured with a rectal probe and maintained at ~37.5°C by means of a heating pad. The trachea was incised in the intercartilaginous area and a tracheotomy tube was inserted. Thereafter the cat was placed in a head holder. A craniotomy was performed over the estimated location of the primary auditory cortex (AI) of the right hemisphere. The opening was further widened with rongeurs until the posterior ectosylvian sulcus was visible. The dura was removed and the cortical surface was protected with a film of silicone oil. For some of the electrophysiological recordings the oil was replaced with a thin layer of agarose to minimize brain pulsations. Anesthesia was maintained throughout the experiment by a continuous infusion of pentobarbital sodium (1-2 mg·kg
1·h1) in lactated Ringer solution (1-2 ml·kg1·h1). In two experiments we replaced the pentobarbital with Ketamine (1-2 mg·kg1·h1) and Diazepam (1-2 mg·kg1·h1) after completion of the surgery. The infusion rate was adjusted according to several criteria that included electrocardiogram, body temperature, and the status of periodically checked reflexes. The cat received an injection of dexamethasone (0.14 mg/kg sc) to prevent brain edema, together with atropine (1 mg/kg) to reduce salivation.
at 1 kHz) were advanced with a hydraulic microdrive (Kopf) to a depth 700-1,200 µm below the cortical surface at different locations of AI. The signals of the electrodes were band-pass filtered (1-3 kHz) and amplified. Action potentials of single neurons or a small group of neurons were separated with triggering devices (Bak Dis-1 and Alpha-Omega Engineering, MSD). In a few occasions in which single- and multiunit activity were simultaneously recorded through the same electrode, the trigger level for the cluster was set such that the cluster recording did not include the action potentials of the single unit. Spike events were sampled with a resolution of 0.03 ms and stored in a computer (DEC 11/73 or IBM compatible). The recording window was in the range of 50 and 400 ms after each trial onset.
t) was always 30 ms shorter than SOA. Although the study focused on nonsimultaneous stimulus interactions, temporally partially overlapping stimuli were also tested in a few cases. The first SOA tested usually was 30 or 50 ms. Thereafter, other SOAs were presented in a random order. Depending on the duration of the two-tone interaction and on how long recordings from single neurons could be maintained, three to nine SOAs were tested per neuron or neural cluster. The effect of the masker on the excitability of the neuron was always tested with the same probe tone, which was usually a CF tone, 10-20 dB above its neural threshold. Between each stimulus pair there was a pause between 350 and 1,030 ms. In a few cases, two-tone interactions were tested with longer masker durations, and with probes at a different intensity of frequency.
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FIG. 1.
Stimulus paradigm. Frequency and intensity of masker as well as stimulus onset asynchrony (SOA) of masker and probe were parametrically varied. Masker and probe duration as well as frequency and intensity of probe were not changed in most experiments. t, interval from masker offset to probe offset.
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FIG. 2.
Method used to assess the extent of masking tuning curves (MTCs). A: number of action potentials of a single cortical unit evoked by different frequency-intensity values of the masker. Six hundred seventy-five different maskers were presented, encompassing 45 frequency values at 15 intensities. The length of the shortest bar is equivalent to 1 action potential. Parameters to describe the extent of the receptive field were minimum threshold, characteristic frequency (CF), and the lower and upper frequency borders 10 and 40 dB above the neuron's threshold ( 
). Star: frequency and intensity of the probe that was used in B. B: responses of a constant probe of 6 kHz and 38 dB (star in A). The probe was always preceded by a masker of variable frequency and intensity and the probe responses are plotted at the frequency-intensity location of the masker. C: low-pass-filtered version of B, with weighting factors as described in METHODS. The size of each rectangle indicates the response probe strength after the presentation of a particular masker, weighted by responses to similar stimuli. Open rectangles: probe responses stronger than 3 times the mean response of the bottom 3 rows. Shaded areas: probe responses that were below the mean response of the bottom 3 rows minus half its SD.
). From this function, the transition point was defined as the point in the rate-intensity function that marked the change from a fast-growing, low-intensity portion to a less fast-growing, saturating, or decreasing high-intensity portion (Schreiner and Mendelson 1990). Monotonicity was defined as the slope of the rate-intensity function above the turning point and was measured in spikes per decibel. The third parameter was the shortest latency of the responses. It was obtained by determining the minimum in the latency-intensity profile at CF for the first spike latency (Schreiner and Raggio 1996). This profile was estimated from three stimulus frequencies at or near CF to eliminate spurious short-latency spontaneous events. Parameters of excitatory receptive fields were estimated from 4-10 stimulus repetitions, because the analysis also included responses to the first tone of the two stimuli.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 3.
Time course of 2-tone interactions for a broadly tuned neuron in the primary auditory cortex. First frame (free standing) of the pseudo-3-dimensional plot shows the neural responses during the presentation of the 1st tone (masker) of 675 different stimulus pairs. Dashed outline: receptive field border. Star: frequency and intensity of the 2nd tone of the pair (probe). The following, connected frames demonstrate the action of maskers of different frequency and intensity on the neural activity of the neuron. The effect of the masker was tested by registering the neural responses to a constant tone burst (probe). Six SOAs were presented (30-350 ms).
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FIG. 4.
Time course of 2-tone interactions for a narrowly tuned single neuron. Same conventions as in Fig. 3.
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FIG. 5.
Time course of 2-tone interactions for a multiunit cluster. Same conventions as in Fig. 3.
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FIG. 6.
Action of maskers on the latency of probe responses for single neurons. A: excitatory subfields of the receptive field (left) were obtained with individual tone bursts; inhibitory subfields (right) were obtained with simultaneous presentation of a constant probe ( 
) and variable masker tone bursts. B: time course of forward inhibition as reflected in the number of evoked action potentials throughout the course of the probe signal. The evoked action potentials were integrated over a range of 10-30 ms after the probe onset. Boxes to the right of each display: latency (mean ± SD) of the 1st action potential of the probe responses (averaged across different frequencies) against the intensity of the preceding masker. C: time course of forward inhibition of probe responses measured over a short latency range (10-20 ms after probe onset). With long-latency responses omitted, the extent of the MTC increases. Shaded lines: MTCs for the long latency range (B) for comparison.
0.13- to 0.168-ms increase in latency per decibel increase in masker intensity. Slope values were significantly higher at a SOA of 30 ms than at SOAs where no magnitude reductions of probe responses were evident. For SOAs >30 ms, no clear dependence of the latency on the masker intensity was seen for most of the neurons. At these time intervals the average latency varied, with a few exceptions, only weakly with the masker intensity.
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FIG. 7.
Time courses of the frequency range of inhibitory maskers for 3 neurons. Abscissa: temporal interval between masker and probe onsets (SOA). Ordinate: distance of the lowest ( 
) and highest (
) inhibitory masker frequency from the neuron's CF, 10 dB (A-C) and 40 dB (D-F) above the excitatory threshold. Values were fitted with a linear regression analysis. Regression coefficients for the high- and low-frequency slope were 0.81 and 0.63 (B), 0.45 and 0.91 (D), 0.10 and 0.74 (E), and 0.80 and 0.87 (F), respectively. Borders of the excitatory receptive field at the same intensities are indicated by the horizontal lines. Shadings in E correspond to 4 different masker-probe interactions. Light gray: probe response is completely suppressed by preceding excitatory masker response. Black: probe is completely suppressed but not preceded by an excitatory masker response. Dark gray: probe magnitude is not suppressed by preceding excitatory response. White: probe is not suppressed and not preceded by excitatory masker response. Diagonal lines: linear regression of the upper and lower frequency boundaries of the inhibited area.
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FIG. 8.
Time courses of the intensity range of inhibitory maskers for 3 neurons. Ordinate: minimal inhibitory masker ( ) and the maximal masker intensity () that inhibited probe responses within the dynamic range tested. Gray horizontal lines: intensity range over which the neuron responded with an excitatory response. In A and B, the highest tested intensities resulted in a response.
; Schreiner et al. 1992). This indicates that most portions of the dorsoventral extent of isofrequency domains were encountered in the present study. Forward inhibition of probe responses was found in 107 cases according to the definition given in METHODS. The criterion for forward inhibition failed for four neurons because neurons did not respond to the probe when it was preceded by maskers at low intensities. Responses of these neurons, however, were facilitated by particular maskers, and thus also exhibited nonsimultaneous two-tone interactions. Thus responsiveness of all neurons in AI depended on the temporal stimulus context.
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FIG. 12.
Comparison of the extent of the receptive field of the neurons (abscissa) with the stimulus range of forward inhibition at an SOA of 30 ms (ordinate). A: minimal inhibitory masker intensity vs. neural threshold. B: maximal inhibitory masker intensity vs. maximal intensity to which the neuron responded. C: frequency of the minimal inhibitory masker vs. CF. D: bandwidth of MTCs 40 dB above neural threshold vs. excitatory bandwidth.
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FIG. 9.
Group results of recovery from forward inhibition. Each plot shows a parameter of the MTC at an SOA of 30 ms on the abscissa and the corresponding parameter at an SOA of 3/4 of the maximal duration of forward inhibition on the ordinate. A: frequency of the minimal inhibitory masker. B: bandwidth of the inhibitory frequency range 40 dB above neural threshold. C: minimal inhibitory masker intensity. Some dots indicate several data points.
4.76, P < 0.001) faster with SOA (2.26 ± 1.65 octaves of masker frequency per decade of SOA) than the higher-frequency boundary of the MTC decreased with SOA (1.24 ± 0.83 octaves/decade). As mentioned above, the frequency of the minimal inhibitory masker intensity did not change with SOA for the majority of neurons.
2 = 0.016, P = 0.90, n = 94). The longest inhibition was induced, in most cases, from maskers around the neuron's CF. Maskers that induced the longest forward inhibition usually had a high intensity. However, for a number of cases maskers of an intermediate intensity were more effective, suggestive of nonmonotonic suppression-level functions. Forward inhibition was shorter lasting for softer maskers and maskers with frequencies different from CF. The dependence of the frequency of the masker can be demonstrated with an example (Fig. 7E). If the masker had a frequency similar to the CF of the neuron and had an intensity 40 dB above neural threshold, the neuron was inhibited for a period of 430 ms. For a different masker frequency just 1 octave below the CF, forward inhibition only lasted for 44 ms. That means that the neuron responded to each tone of a stimulus pair if the frequencies of the two tones were different, whereas it responded to the first tone only when the tones were the same. The average dependence of forward inhibition duration on the frequency difference of the masker and the probe is displayed in Fig. 11. It was calculated from the decrease of the frequency range of MTCs 40 dB above excitatory threshold and the maximal duration of forward inhibition.
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FIG. 10.
Maximal duration of forward inhibition. For each single-unit and multiunit recording, the maximal duration of forward inhibition was obtained. Mode: 120 ms. Mean: 143 ± 71 (SD) ms.
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FIG. 11.
Dependence of the duration of forward inhibition on the frequency separation of the masker and the CFs 40 dB above neural threshold. Positive and negative values: masker frequencies above and below CF, respectively. Positive values were based on 61 cases and negative values on 58 cases. The maximal duration of forward inhibition for masker and probe of identical frequency was slightly higher than for the larger sample displayed in Fig. 11.
3.91, P = 0.0001). MTCs were, at this SOA, always V shaped, irrespective of the shape of the receptive field. The frequency of the minimal inhibitory masker intensity was similar to the CF of the neuron, both for single units (n = 43, Z = 1.222, P = 0.222) and multiunits (n = 51, Z = 0.769, P = 0.442). The bandwidth of MTCs 40 dB above neural threshold grew monotonously for louder maskers and was, on average, larger than corresponding values of the excitatory regions of the receptive field. The difference was highly significant for single-unit activity (n = 30, Z = 4.19, P < 0.0001) and the same tendency was seen for multiunit activity (n = 30, Z = 1.74, P = 0.08). In addition, a small asymmetry of MTCs was seen: MTCs extended 0.5 octaves further to the low-frequency site than the receptive field, whereas the difference was 0.3 octaves on the high-frequency site (n = 60, Z = 3.680, P = 0.0002). The width of MTCs at an SOA of 30 ms was also compared with the extent of the total receptive field 40 dB above neural threshold. Total receptive fields included both excitatory and inhibitory subfields. Inhibitory subfields were measured for 23 single units by simultaneously presenting a probe tone (see METHODS). Almost half of the neurons had MTCs that extended beyond the total receptive field. This indicates that forward inhibition was not only induced from unequivocal excitatory and inhibitory regions of the receptive field, but, for the majority of neurons, even from stimuli outside the classical receptive field. However, on average there was no difference between both the lower (Z = 0.00, P = 1) and upper (Z = 1.00, P = 0.32) frequency limits of the MTC and the respective values of the total receptive field.
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TABLE 1.
Relation of temporal charactersitics of forward inhibition and various receptive field properties
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FIG. 13.
Action of maskers of different duration on probe responses. A: neuron's receptive field and the location of the probe (2 kHz, 37.5 dB; ). B-D: forward inhibition for different SOA and probe delays. B and C: probe responses after the presentation of short maskers (30 ms in duration) at 2 SOAs (30 and 190 ms, respectively). D: probe responses are displayed after the presentation of a long masker and at a long SOA (both 190 ms).
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TABLE 2.
Comparison of parameters of receptive field and MTC for simultaneously recorded single neurons and multiunit clusters
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, who studied two-tone interactions with a similar paradigm. Thus the results of the present study provide a confirmation of the findings of Calford et al. The following discussion focuses mainly on new findings, i.e., the time course of forward inhibition, its relation to static receptive field properties, and the comparison of single- and multiunit data. Before we attempt an appropriate interpretation of these results, we first consider some potential effects of the experimentation techniques.
found that about two-thirds of the neurons in the auditory cortex can have reduced responses if the interstimulus interval is <1.6 s. Thus our study assessed relative forward inhibition with respect to a habituated state (see also Sutter and Schreiner 1991). Beyond the longest onset interval between masker and probe at which forward inhibition was measured, responses to the probe were still below the value without any preceding sound. The maximal duration of forward inhibition thus represents the longest SOA at which forward inhibition depended on the frequency and intensity of the masker. We did not extend the intertrial interval between the presentation of the stimulus pairs to values >1.6 s because of time restrictions. In some cases stimulus interactions for particular SOAs were repeated with a different intertrial interval. In all of these cases MTCs were independent of the intertrial interval.
). The single presentation of randomized tones for the assessment of tuning curves was chosen because it shows little adaptation effect, covers a wide range of tone configurations, and allows post hoc evaluation of the entire response area. The low statistics of the responses to particular tones can be improved by local pooling. This method has the advantage that different aspects of interest can be emphasized, e.g., by averaging only over responses to neighboring frequencies or intensities. In the present investigation, two procedures were applied to arrive at more reliable estimates of MTCs. First, stimulus response areas were low-pass filtered. This procedure was reasonable because most probe response areas could be divided into two main regions. There was one region, usually in the center of the stimulus response area, in which no responses to the probe were present. This central region was surrounded by another region where response strength was not affected by the preceding masker. The transition between the two regions appeared sharp, although we could not determine it accurately. The range of this transition zone was more quantitatively measured by Calford and Semple (1995), who, over a limited frequency and intensity range, presented each masker/probe pair 20 times. Although no values were given, the figures of Calford and Semple indicate that the transition zone was between 0.2 and 0.4 octaves wide. Thus probe response areas basically consisted of two homogenous regions. Within each region, average response strength to particular probes could be estimated by pooling the responses to stimuli that differed only slightly from the stimulus under consideration. After low-pass filtering, those probe responses were labeled as being inhibited where the response strength was below a certain value. Because of the low-pass filtering, we could select a quite liberal criterion for forward inhibition, which was a reduction of the response strength below half the SD of the average response strength of the habituated state. Sizes and shapes of MTCs were quite robust within a reasonable range of criteria and were similar to those derived by visual inspection of probe response areas. The varianceof MTCs could be reduced further because forward inhibition was measured at different SOAs. This enabled us to compare individual MTC and to discard obvious outliers. In addition, a regression analysis could be performed on the temporal development of various parameters of MTCs, which provided a better estimate of the shape of individual MTCs. Taken together, the quantitative procedures employed in the present study revealed reasonably accurate MTCs. Excitatory subregions of receptive fields were assessed at a higher confidence level than MTCs because stimuli were presented 4-10 times (responses to the masker in the various 2-tone conditions were included for this analysis).
-aminobutyric acid-A (GABAA) receptors (Franks and Lieb 1994). Therefore the temporal response characteristics of cortical cells obtained in this study have to be considered carefully. A way to estimate the potential influence of the anesthesia is to compare the temporal dynamics obtained with different anesthetic drugs. Two of our experiments (10 neurons) were performed with the use of ketamine (supplemented by azepromacine). Between the two types of anesthesia no obvious difference in any of the spectrotemporal characteristics of forward inhibition was observed. Similar results were reported by Calford and Semple (1995), who studied two-tone interaction with the same drugs. Thus the results of the present study are consistent between the anesthetics used throughout the experiment. Recordings of neural discharges from awake guinea pigs (Creutzfeldt et al. 1980) and recordings of intracortical slow-wave activity in cats (Etholm et al. 1976) have shown that, in awake preparations, forward inhibition is also present, although time constants may be shorter and strength of inhibition may be weaker. To what extent the results of the present study on other properties of forward inhibition apply to unanesthetized animals, however, still remains to be determined.
1 h. Single-unit recordings frequently could not be maintained over such long periods. Therefore recordings of multiunit activity provided a way to study forward inhibition in more detail and to record from more cortical locations so that the data base was increased.
).
; Smith 1977). Consequently it is seen only for stimuli within the excitatory receptive field of the neuron. This and previous studies (Calford and Semple 1995; Phillips et al. 1989) have found that a significant number of neurons was inhibited from stimuli outside their excitatory receptive field, indicating that adaptation effects from subcortical stages of the auditory pathway, including the auditory nerve, cannot be the sole sources of the observed effects. Forward inhibition of the activity of cortical cells may reflect inhibitory properties already present at subcortical stages of the auditory pathway as well as cortical influences. Numerous studies have demonstrated that forward inhibition of neural responses is present on all levels of the auditory system, beginning with the cochlear nuclear complex (Boettcher et al. 1990; Kaltenbach et al. 1993; Shore 1995), up to the medial geniculate body (Schreiner 1981). At successive stages of the auditory pathway, new properties of forward inhibition emerge. In the cochlear nuclear complex, ~20% of the neurons are inhibited from stimuli outside the excitatory subfields of their receptive field. In addition, there are neurons with nonmonotonous time courses of forward inhibition (Kaltenbach et al. 1993; Shore 1995). For these neurons, suppression of the probe response was not present until several tens of milliseconds after the masker offset. In the medial geniculate body there is evidence that neurons can also be inhibited from stimuli outside the receptive field (Schreiner 1981). Thus, with regard to the observed stimulus range of forward inhibition, subcortical neurons could already account for the properties of cortical neurons.
). Similar values were also found for the chinchilla (Harris and Dallos 1979). For the anteroventral cochlear nucleus, Shore (1995) reported slightly longer recovery times than in the auditory nerve. In the medial geniculate body of awake guinea pigs, the recovery time constants were found to be up to twice the time constants of those found in the auditory nerve (Schreiner 1981). In our study the maximal duration of forward inhibition was in the range of 40 and 430 ms, with a mean of 143 ms, and thus not much longer than in subcortical stages of the auditory pathway. Different time constants, however, have to be considered carefully. First, in all neural structures that have been investigated so far, forward inhibition has been studied with maskers of different intensity, frequency, and duration. Second, studies have been performed on different species and under different anesthesia. Therefore, with regard to the duration of forward inhibition, no conclusion can be drawn as to the origin of cortically revealed forward inhibition.
). Neurons in the auditory nerve can phase lock their responses to modulation rates >1,000 Hz (Joris and Yin 1992), whereas in cortical auditory fields, most neurons have cutoff frequencies of ~10 Hz (Creutzfeldt et al. 1980; Eggermont 1994; Schreiner and Urbas 1986, 1988). Thus studies with amplitude- and frequency-modulated sounds indicate that cortical mechanisms contribute to the generation of temporal response properties of cortical neurons.
), exhibit only a gradual suppression of neural discharges, most cortical neurons are completely inhibited after a masker stimulus. Thus, in conclusion, there is evidence that the forward inhibition of cortical neurons is generated, in part, by intracortical mechanisms (see also Calford and Semple 1995). This view is further supported by a study of visual forward masking that compared temporal stimulus interactions in the lateral geniculate body and the visual cortex (Nelson 1991a,b).
, 1990; Phillips and Cynader 1985; Phillips and Sark 1991), who found with simultaneous tone interactions that reduction of responsiveness and prolongation of response latencies are due to adaptation (e.g., Fig. 6), whereas no significant changes of latencies are seen when a cell receives competing excitatory and inhibitory inputs. Adaptation, however, cannot account for all the forward inhibition effects observed in cortical cells, because it was also induced from maskers to which the neuron under consideration did not respond. Thus inhibitory postsynaptic potentials also have to be involved in the cortical forward inhibition.
). This view is further supported by our finding that there was no obvious difference in the properties of forward inhibition between the neurons that were investigated under barbiturate and ketamine anesthesia, although barbiturates are known to potentiate the effect of GABAA receptors (Franks and Lieb 1994). Results thus are indicative of presynaptic inhibition, possibly at the geniculate-cortical synapse, or of shunting inhibition at the cell soma. This temporal inhibition possibly provides a mechanism similar to "spatial" lateral inhibition. Whereas this type of inhibition suppresses the activity of adjacent neurons and thus enhances the spatial contrast, the former suppresses neural activity of successive time intervals and thus sharpens the temporal contrast.
; Eggermont 1991, 1994; Müller-Preu
1986; Phillips et al. 1989; Schreiner and Urbas 1986, 1988; but see deRibaupierre et al. 1972). The present study shows that maximal duration of forward inhibition, however, depended strongly on the spectral composition of consecutive elements. Forward inhibition lasted the longest if successive tones had the same frequency and were at the CF of the neuron. Duration of forward inhibition, however, was significantly shorter if successive elements differed in frequency, even if they were still clearly inside the excitatory receptive field. Because modulation transfer functions have mostly been determined with CF tones, they only describe the lower limits to which cortical neurons can encode modulated sounds. For sounds in which not only does the envelope vary over time but also the spectral composition changes in time, results of the present study indicate that neurons can encode sounds with modulation rates above those predicted by the cutoff frequency of the traditional modulation transfer function.
). Recently, studying nonsimultaneous two-tone interactions in AI of anesthetized cats, Calford and Semple (1995) reported of several neurons for which MTCs decreased in size as the masker-to-probe-onset interval increased, similar to the present findings.
reported that numerous neurons entrain their discharges to higher modulations the higher the total intensity of the stimulus. This behavior was mostly found for neurons with monotonic rate-intensity functions. For neurons with nonmonotonic rate-intensity functions, however, increasing the stimulus intensity could result in a decrease of the modulation rate to which a neuron responded. These findings were confirmed and extended by Calford and Semple (1995) and the present study: with sequences of tones of different intensity, the longest-lasting forward inhibition was not always induced from the most intense maskers. For a significant number of neurons, maskers at intermediate intensities induced longer periods of inhibition than loud maskers. Calford and Semple concluded that the sources for inhibition responsible for nonmonotonic rate-intensity functions and forward inhibition (at least for long SOAs) are not necessarily identical.
). Long maskers induced longer periods of forward inhibition than did short maskers. That means that neurons respond with higher discharge rates to a sound that is modulated at a particular repetition rate if duration of the elements of the sequence is short and pauses are long than if stimulus duration is long and pauses are short. Another dependence on the modulation envelope has already been uncovered with periodically modulated sounds. It was found that best modulation frequencies are the higher the sharper are the transients of the modulator (Eggermont 1994; Schreiner and Urbas 1988). Influence of slope characteristics of the masker and probe were not investigated in the present study, but these probably also affected the duration of forward inhibition.
, using trains of tone bursts, found that the latency of the first spike response to each tone increased when the temporal interval between the tones was decreased. Similar results were reported for sequences of tone bursts of different frequency and intensity (Calford and Semple 1995; present study) and for click trains (Eggermont 1991). In all of these studies latency increases were associated with a decreased neural discharge probability. In addition to previous reports on temporal stimulus interactions, the present study found cases for which the latencies of neural responses were lengthened without concomitant alterations of the response strength (e.g., Fig. 4). This indicates that rate and latency of neural discharges can vary independently of each other. Thus discharge rate and timing of discharges could also provide independent neural mechanisms for the encoding of time-varying sounds.
). A combined approach provides the concept of the spectrotemporal receptive field, which is derived from a calculation of a linear function of the second-order Volterra kernel for a special class of stimuli (Aertsen and Johannesma 1980). For cortical neurons the relation between the spectral and temporal aspects of receptive fields has, with a few exceptions, not yet been established.
). Because in subcortical stages of the auditory pathway duration of forward inhibition is independent of the neuron's CF, results suggest that cortical neurons may be involved in generating perceptual forward masking effects.
; Schreiner et al. 1992). Our findings therefore could indicate that there are functionally specialized neurons in AI that have a high spectral and temporal resolution and that respond shortly after the presentation of a stimulus, and that there are other neurons that integrate stimuli over a wider spectral and temporal range and have long latency periods. A similar relationship has also been observed in a cortical study of repetition coding of acoustic and electrical cochlear stimulation in which best following rate and onset latency were inversely correlated (Schreiner and Raggio 1996). Further evidence comes from recordings from the auditory midbrain in which the latency of neural responses was negatively correlated with the preferred modulation rate (Langner et al. 1987). In conclusion, these findings suggest that the association between the latency of neural responses and the duration of temporal stimulus interactions provides a facilitation for the processing of time-varying sounds.
, 1994; Rajan et al. 1990; Schreiner and Mendelson 1990; Schreiner et al. 1992). In the present study we found that the bandwidth was weakly correlated with several temporal aspects of response characteristics of cortical neurons, including maximal duration of forward inhibition and temporal course of the minimal inhibitory masker intensity and of inhibitory frequency range (Table 1). Results of the present study thus give rise to the speculation that temporal response characteristics of neurons are also topographically organized within AI. This hypothesis is further supported by an investigation of some of the authors who studied stimulus interactions with sequences of five tone bursts with different temporal intervals between the elements of the sequence (Krüger and Schreiner 1994). It was found that neurons in the ventral third of the isofrequency domain had shortest recovery periods, whereas recovery was longer for neurons that were located more ventrally and dorsally.
). Similar dependencies have been described for rhythmic grouping of tone sequences and stream segregation and integration of sequences (reviewed in Bregman 1990). How these changes of the neural activity in the cortex are involved in the generation of these perceptions and their role in the analysis of complex auditory scenes, however, still remains an open question.
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ACKNOWLEDGEMENTS |
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We thank Dr. Barbara Calhoun and S. Wong for help during some of the experiments.
This work was supported by the Office of Naval Research (N00014-94-1-0547) National Institute of Deafness and Other Communications Disorders Grant DC-22260, and Deutsche Forschungsgemeinschaft (Br 1385/1).
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FOOTNOTES |
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Present address and address for reprint requests: M. Brosch, Institut für Neurobiologie, Brenneckestrae 6, 39118 Magdeburg, Germany.
Received 28 December 1995; accepted in final form 24 October 1996.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
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M. P. Kilgard and M. M. Merzenich Order-sensitive plasticity in adult primary auditory cortex PNAS, March 5, 2002; 99(5): 3205 - 3209. [Abstract] [Full Text] [PDF]
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R. L. Jenison, J. W. H. Schnupp, R. A. Reale, and J. F. Brugge Auditory Space-Time Receptive Field Dynamics Revealed by Spherical White-Noise Analysis J. Neurosci., June 15, 2001; 21(12): 4408 - 4415. [Abstract] [Full Text] [PDF]
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M. Brosch and C. E. Schreiner Sequence Sensitivity of Neurons in Cat Primary Auditory Cortex Cereb Cortex, December 1, 2000; 10(12): 1155 - 1167. [Abstract] [Full Text] [PDF]
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J. J. Eggermont Neural Responses in Primary Auditory Cortex Mimic Psychophysical, Across-Frequency-Channel, Gap-Detection Thresholds J Neurophysiol, September 1, 2000; 84(3): 1453 - 1463. [Abstract] [Full Text] [PDF]
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T. Lu and X. Wang Temporal Discharge Patterns Evoked by Rapid Sequences of Wide- and Narrowband Clicks in the Primary Auditory Cortex of Cat J Neurophysiol, July 1, 2000; 84(1): 236 - 246. [Abstract] [Full Text] [PDF]
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R. A. Reale and J. F. Brugge Directional Sensitivity of Neurons in the Primary Auditory (AI) Cortex of the Cat to Successive Sounds Ordered in Time and Space J Neurophysiol, July 1, 2000; 84(1): 435 - 450. [Abstract] [Full Text] [PDF]
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M. I. Sanderson and J. A. Simmons Neural Responses to Overlapping FM Sounds in the Inferior Colliculus of Echolocating Bats J Neurophysiol, April 1, 2000; 83(4): 1840 - 1855. [Abstract] [Full Text] [PDF]
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A. V. Galazyuk, D. Llano, and A. S. Feng Temporal Dynamics of Acoustic Stimuli Enhance Amplitude Tuning of Inferior Colliculus Neurons J Neurophysiol, January 1, 2000; 83(1): 128 - 138. [Abstract] [Full Text] [PDF]
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M. Brosch, A. Schulz, and H. Scheich Processing of Sound Sequences in Macaque Auditory Cortex: Response Enhancement J Neurophysiol, September 1, 1999; 82(3): 1542 - 1559. [Abstract] [Full Text] [PDF]
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D. V. Buonomano and M. M. Merzenich Net Interaction Between Different Forms of Short-Term Synaptic Plasticity and Slow-IPSPs in the Hippocampus and Auditory Cortex J Neurophysiol, October 1, 1998; 80(4): 1765 - 1774. [Abstract] [Full Text] [PDF]
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 R. C. deCharms, D. T. Blake, and M. M. Merzenich Optimizing Sound Features for Cortical Neurons Science, May 29, 1998; 280(5368): 1439 - 1444. [Abstract] [Full Text]
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