Single-neuron responses to rapidly presented temporal sequences in the primary auditory cortex of the awake macaque monkey

One fundamental process of the auditory system is to process rapidly occurring acoustic stimuli, which are fundamental components of complex stimuli such as animal vocalizations and human speech. Although the auditory cortex is known to subserve the perception of acoustic temporal events, relatively little is currently understood about how single neurons respond to such stimuli. We recorded the responses of single neurons in the primary auditory cortex of alert monkeys performing an auditory task. The stimuli consisted of four tone pips with equal duration and interpip interval, with the first and last pip of the sequence being near the characteristic frequency of the neuron under study. We manipulated the rate of presentation, the frequency of the middle two tone pips, and the order by which they were presented. Our results indicate that single cortical neurons are ineffective at responding to the individual tone pips of the sequence for pip durations of <12 ms, but did begin to respond synchronously to each pip of the sequence at 18-ms durations. In addition, roughly 40% of the neurons tested were able to discriminate the order that the two middle tone pips were presented in at durations of > or =24 ms. These data place the primate primary auditory cortex at an early processing stage of temporal rate discrimination.     

The Startle Eyeblink Response to Low Intensity Acoustic Stimuli

Four experiments were conducted to investigate the acoustic startle response to stimuli of low intensities. Eyeblink responses (integrated EMG from orbicularis oculi) were measured from male and female college students. Experiment 1 compared tone and noise stimuli varying in intensity (50 and 60 dB(A) SPL), with noise stimuli producing greater response amplitude and probability than tone stimuli. Experiment 2 was designed to investigate temporal summation of low intensity stimuli using single and paired 70dB(A) SPL broadband noises, and an onset-to-onset interval between the brief stimuli in a pair equal to the duration of the single stimuli. Increasing the duration of single stimuli resulted in larger responses, illustrating temporal summation. Experiment 3 used 60 and 70 dB(A) SPL broadband noise varying in rise/fall time, with faster-rising stimuli producing larger responses, and more intense stimuli producing larger and more probable responding. Experiment 4 employed the startle modification paradigm using 60 and 70 dB(A) SPL broadband noises as startle stimuli and a 50dB(A) SPL tone as a prepulse. Response amplitude and probability to both 60 and 70 dB(A) SPL stimuli were significantly inhibited by the 50dB(A) SPL prepulse. These studies show that the acoustic startle response is more sensitive than previously thought, and the elicitation of startle by low intensity stimuli argues against the limitation of the startle reflex as a high intensity phenomenon. These findings can increase the application of this response system by showing that startle stimuli need not be of high intensity, because reliable and differential startle can be elicited and modified at relatively low stimulus intensities.     

Developmental change in auditory selective attention as reflected by phasic heart rate changes

Heart rate was recorded from five different groups of children (ages 7, 10, 12, 14, and 20 years) while they were performing an auditory selective attention task. The participants were instructed to count rare tone pips embedded in a series of standard tone pips presented at one (attended) ear while ignoring rare and standard stimuli presented at the other (unattended) ear. A pattern of anticipatory heart rate deceleration followed by acceleration was associated with rare tone pips at the attended ear but not with rare tone pips that should be ignored. The absence of differential sensitivity of heart rate responses to rare tone pips presented at the unattended ear was observed for all age groups. These findings were interpreted to suggest that the ability to ignore irrelevant target stimuli has reached mature levels during middle childhood. The depth of anticipatory deceleration increased until age 14, suggesting that the ability to maintain attentional set continues to develop beyond childhood.     

Psychopathy and Selective Attention During Performance of a Complex Perceptual-Motor Task

Autonomic and electrocortical activity were recorded while prison inmates with high (H) and low (L) ratings of psychopathy were presented with a series of binaural tone pips, either by themselves (passive attention) or while video games were being played (selective attention). During selective attention the subjects were told that the tone pips were irrelevant to the primary task, the video games. The N100 component of the auditory evoked potential was used as an index of attention paid to the tone pips, while performance on the video games was considered to be a reflection of attentiveness to the primary task. There were no group differences in N100 amplitude or latency during passive attention, supporting the results from several previous studies. During selective attention Group H gave small N100 responses to the tone pips during each video game trial, including the first one, while Group L gave large N100 responses to the tone pips during the first trial, and small responses during later trials. Both groups performed equally well during the first few trials, but while the performance of Group L continued to improve, that of Group H deteriorated over the last few trials. The results were interpreted in terms of limited capacity models of attention, and provided some support for the hypothesis that psychopaths allocate a relatively large proportion of their attentional resources to things of immediate interest, effectively ignoring other stimuli.     

Physiological response properties of neurons in the superior paraolivary nucleus of the rat

The superior paraolivary nucleus (SPON) is a prominent nucleus of the superior olivary complex. In rats, this nucleus is composed of a morphologically homogeneous population of GABAergic neurons that receive excitatory input from the contralateral cochlear nucleus and inhibitory input from the ipsilateral medial nucleus of the trapezoid body. SPON neurons provide a dense projection to the ipsilateral inferior colliculus and are thereby capable of exerting profound modulatory influence on collicular neurons. Despite recent interest in the structural and connectional features of SPON, little is presently known concerning the physiological response properties of this cell group or its functional role in auditory processing. We utilized extracellular, in vivo recording methods to study responses of SPON neurons to broad band noise, pure tone, and amplitude-modulated pure tone stimuli. Localization of recording sites within the SPON provides evidence for a medial (high frequency) to lateral (low frequency) tonotopic representation of frequencies within the nucleus. Best frequencies of SPON neurons spanned the audible range of the rat and receptive fields were narrow with V-shaped regions near threshold. Nearly all SPON neurons responded at the offset of broad band noise and pure tone stimuli. The vast majority of SPON neurons displayed very low rates of spontaneous activity and only responded to stimuli presented to the contralateral ear, although a small population showed binaural facilitation. Most SPON neurons also generated spike activity that was synchronized to sinusoidally amplitude-modulated tones. Taken together, these data suggest that SPON neurons may serve to encode temporal features of complex sounds, such as those contained in species-specific vocalizations.     

Temporal plasticity in the primary auditory cortex induced by operant perceptual learning

Processing of rapidly successive acoustic stimuli can be markedly improved by sensory training. To investigate the cortical mechanisms underlying such temporal plasticity, we trained rats in a 'sound maze' in which navigation using only auditory cues led to a target location paired with food reward. In this task, the repetition rate of noise pulses increased as the distance between the rat and target location decreased. After training in the sound maze, neurons in the primary auditory cortex (A1) showed greater responses to high-rate noise pulses and stronger phase-locking of responses to the stimuli; they also showed shorter post-stimulation suppression and stronger rebound activation. These improved temporal dynamics transferred to trains of pure-tone pips. Control animals that received identical sound stimulation but were given free access to food showed the same results as naive rats. We conclude that this auditory perceptual learning results in improvements in temporal processing, which may be mediated by enhanced cortical response dynamics.     

Somatosensory input to auditory association cortex in the macaque monkey

We investigated the convergence of somatosensory and auditory inputs in within subregions of macaque auditory cortex. Laminar current source density and multiunit activity profiles were sampled with linear array multielectrodes during penetrations of the posterior superior temporal plane in three macaque monkeys. At each recording site, auditory responses to binaural clicks, pure tones, and band-passed noise, all presented by earphones, were compared with somatosensory responses evoked by contralateral median nerve stimulation. Subjects were awake but were not required to discriminate the stimuli. Borders between A1 and surrounding belt regions were identified by mapping best frequency and stimulus preferences and by subsequent histological analysis. Regions immediately caudomedial to A1 had robust somatosensory responses co-represented with auditory responses. In these regions, both somatosensory and auditory response profiles had "feedforward" patterns; initial excitation beginning in Lamina 4 and spreading to extragranular laminae. Auditory and somatosensory responses displayed a high degree of temporal overlap. Anatomical reconstruction indicated that the somatosensory input region includes, but may not be restricted to, the caudomedial auditory association cortex. As was earlier reported for this region, auditory frequency tuning curves were broad and band-passed noise responses were larger than pure tone responses. No somatosensory responses were observed in A1. These findings suggest a potential neural substrate for multisensory integration at an early stage of auditory cortical processing.     

Increased motor excitability produced by alerting stimuli

The proposal that increased excitability of sensory and motor systems occurs in response to dishabituated sensory stimuli was supported by experiments with cats in which excitability was measured by the amplitude of the response evoked by an electrical test stimulus. Evoked EMG, evoked head movement and the postsynaptic visual cortex response were briefly augmented following such stimuli, with a latency less than 20 msec for auditory and less than 50 msec for visual stimuli. Evoked EMG responses were rare during habituation, but even faint stimuli (40 db (SPL) tone pips) were effective during conditioning procedures. The proposed organization of the brain was thought to have adaptive significance, helping the subject to cope with emergency situations by enhancing the processing of sensory and motor information.     

Azimuthal processing in the posterior auditory thalamus of cats.

The responses to free-field acoustic stimuli of 157 units in the auditory thalamus of anesthetized cats were studied in relation to the localization of pure tone stimuli in the azimuthal plane. Units were classified as 'directional' if their firing rates at sound levels in excess of 20 dB above threshold varied by more than 50% as a function of azimuth. Sixty-five % of the units in the nucleus of the brachium of the inferior colliculus and 30% in the ventral division of the medial geniculate body were found to be directional, suggesting different processing channels for sound localization between colliculus and cortex.     

The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey (Saimiri sciureus)

Summary Action potentials of single auditory cortical neurons of the squirrel monkey were recorded in a chronic, unanesthetized preparation. The responsiveness of units was tested with various types of simple and complex acoustic stimuli in a free field situation. As simple auditory stimuli, bursts of pure tones, clicks, and white noise were utilized. Species-specific vocalizations served as complex, biologically significant stimuli.The data are based on 48 neurons which showed a discrete response to speciesspecific vocalizations. In 63% the response to calls could be predicted from the units' responses to simple stimuli. Thirty-seven percent of the neurons were classified as unpredictable with respect to their responsiveness to vocalizations. The response of most units was restricted to call stimuli which showed similarities in their frequency-time characteristics. About 7% of the 116 units responding to calls were classified as selective responders because they were not excited by any other stimulus tested. It was not possible to single out the acoustic features to which these units responded.Peter Winter died in an skiing accident in March, 1972.     

Auditory nerve fiber response to wide-band noise and tone combinations.

1. Responses of single auditory nerve fibers to combinations of noise and tone were obtained. The results were found to depend on the relative effectiveness of each stimulus when presented alone. 2. When the response rate to one stimulus presented alone was considerably greater than the response rate to the other stimulus presented alone, the more effective stimulus dominated the responses when the two stimuli were combined. The more effective stimulus captured the response of the neuron. Thus, intense noise was found to mask responses to weaker tones, and intense tones were found to mask responses to weaker noise. This masking of the weaker stimulus is thought to enhance the signal-to-noise ratio of the most prominent response component. 3. When the two stimuli had similar effectiveness, complex interactions occurred. When the tone was near best (characteristic) frequency, partial summation effects occured. The tone partially suppressed the responses to the noise if other frequencies were used. Tones above best frequency caused particularly powerful suppression. 4. The bandwidth of the noise was varied somewhat. While bandwidth affected the effectiveness of the noise, it did not affect the types of interactions observed. 5. For a neuron which was essentially silent in the absence of acoustic stimuli, adding a weak level of noise lowered the threshold of responsiveness to the tone.     

Feature extraction and tonotopic organization in the avian auditory forebrain

Summary In a neurophysiological study within the auditory centers of the mediocaudal telencephalon of the starling, 601 neurons were tested for auditory responses. 369 of these units responded to pure tones, noise bands, amplitude modulations (AM), or species-specific sounds. Of all the auditory neurons, 16.8% did not respond to pure tones but only to more complex stimuli (tone-unresponsive-, TU-units). The remaining auditory units were classified as tone-responsive (TR-units). In 44.3% of TR-units (i.e. 36.9% of all auditory units) differing responses to tones versus more complex stimuli were observed. Responses as they occur in TU-units and in the differing responses of TR-units can be explained by neuronal extraction of features in the time (108 out of 198 neurons) and in the spectral domain (82 out of 198 neurons). Responses to species-specific sounds usually can be explained in terms of extraction of these features. Among neurons sensitive to temporal features, exclusive responses to a narrow range of AM frequencies were observed. In those TU-units that represent spectral features some restrict their responses to noise bands with distinct bandwidths centered around a specific midfrequency. These units reject both wider and narrower noise bands. A tonotopic arrangement of auditory units is found in field L, the surrounding neostriatum (NCM), and the Hyperstriatum ventrale (HV). Isofrequency lines run as a continuum through NCM, field L, and the caudal part of HV. TU-units are integrated into the tonotopic gradient according to the midfrequency of effective stimuli (e.g. noise bands or AM). The anatomical position of auditory units is correlated to their response properties. Within one isofrequency contour an increase in response selectivity is seen from field L to the postsynaptic areas in the NCM and the HV. The results are discussed in terms of possible mechanisms of feature extraction in the avian auditory system.Part of the program of the Sonderforschungsbereich 114 (BIONACH) funded by the Deutsche Forschungsgemeinschaft     

Effects of OFF-BF tones on responses of chopper units in ventral cochlear nucleus. I. Regularity and temporal adaptation patterns.

1. We have recorded the responses of neurons in the anteroventral cochlear nucleus (AVCN) of barbiturate-anesthetized cats to pure tones [either at the unit's best frequency (BF) or at another frequency (OFF-BF)] and to two-tone combination stimuli. 2. The effects of OFF-BF input (either alone or presented simultaneously with a BF tone in a two-tone stimulus) on the response patterns of choppers may include not only rate inhibition but changes in the discharge regularity and the temporal adaptation properties of the spike trains. 3. In the majority of cases we studied (119 of 146 frequencies examined in 45 units), the discharge regularity of a response to an OFF-BF or two-tone stimulus is comparable with that of a "rate-matched" BF tone response. In a minority of cases (27 of 146 frequencies examined), however, OFF-BF input (either alone or in a two-tone stimulus format) changed the regularity compared with that of a rate-matched BF tone response. 4. In the majority of cases studied (139 of 171 frequencies examined in 53 units), the initial pattern of rate adaptation ["temporal adaptation pattern" (TAP)] was the same in response to a short tone burst at BF, to an OFF-BF tone burst, or to a pair of tones. The TAP can, however, be significantly altered by OFF-BF input, although this is a comparatively infrequent occurrence in our data sample (32 of 171 frequencies examined), from the response to BF tone to the response to the two-tone or OFF-BF stimulus, are as follows: sustained to slowly adapting; slowly adapting to transiently adapting, and transiently adapting to slowly adapting. Changes in the TAPs of chopper unit responses have been recorded from both regular and irregular choppers and cannot be accounted for on the basis of changes in sustained firing rate. These changes in the discharge regularity and TAP in the small minority of cases suggest that (at least in these cases) the inhibitory effect of OFF-BF input is not simply the result of two-tone suppression at the level of the auditory nerve fiber input. 5. We have observed that regular choppers may be transformed into irregular choppers by OFF-BF (rate inhibitory) input.(ABSTRACT TRUNCATED AT 400 WORDS)     

Does the heart know what the ears hear? A heart rate analysis of auditory selective attention

Between- and within-channel auditory selective attention were examined by presenting subjects with tone pips randomly to opposite ears; some pips had a slightly different pitch. Subjects were instructed to count rare, deviant tone pips at one ear and ignore all input to the other ear. Heart rate was sampled twice: once for the attended tone pips and once for the nonattended stimulus series. Heart rate responded differently to attended tone pips. While subjects were waiting for the rare stimulus to occur, heart rate slowed until the deviant stimulus was detected, which was followed by heart rate acceleration. Anticipatory heart rate deceleration was largely absent for nonatended series, and rare tone pips presented at the nonattended ear were not followed by acceleratory recovery. All tone pips elicited cardiac cycle time effects, that is, stimuli presented at short delays after the R wave prolonged the concurrent interbeat interval more than stimuli presented later. The cardiac cycle time effect was not altered by stimulus relevance (attended vs. nonattended) or significance (standard vs. rare). These results suggest that all stimuli receive preliminary perceptual analysis, but only attended stimuli are processed for further evaluation.     

Rate-level functions of neurons in the inferior colliculus of cats measured with the use of free-field sound stimuli

1. The responses as a function of stimulus level of 125 single units in the inferior colliculus of anesthetized cats were studied with the use of free-field acoustic stimuli. 2. The characteristic frequency (CF; frequency at which threshold was lowest) of each unit was determined, and stimuli were presented from one of three speaker positions: 45 degrees contralateral to the midline, midline, and 45 degrees ipsilateral to the midline. 3. For each unit a variety of stimulus levels was presented at CF, and the total spike count was summed for 20 stimuli at each level. If time permitted, a similar series of levels of noise was presented. 4. Four classes of rate-level (RL) functions were observed. Monotonic increases in firing rate were observed in 10% of units stimulated with CF stimuli and 57% of units studied with noise. Nonmonotonic RL functions, for which firing first increased and then declined to less than 50% of the peak level, were observed in 61% of units responding to CF tones and in 10% responding to noise. Plateau functions, with shapes lying between these, accounted for 19% of CF responses and the remaining units excited by noise. Some very complex shapes that could not be categorized into the above groups were seen in the remaining 10% of the units responding to CF stimuli. 5. The RL functions of units studied with both noise and CF tones could belong to different classes; commonly, nonmonotonic RL functions to tones were associated with monotonic RL functions to noise. The noise thresholds averaged 10 dB, some 10-20 dB less sensitive than those to CF stimuli. 6. For the vast majority of both noise and tone responses, stimuli from the contralateral location were more effective than those from the other two positions in terms of a lower threshold, higher peak discharge rate, and, for nonmonotonic units, a lower sound level at which the function became nonmonotonic (turnover point). 7. The turnover points of nonmonotonic functions at any given CF could be spread broadly but, overall, tended to be concentrated between -6 and 44 dB. 8. The dynamic ranges (range of levels over which firing rate increased) were larger for monotonic and plateau functions than for nonmonotonic functions, which had dynamic ranges less than 45 dB. The median dynamic range for units stimulated with CF tones was 20 dB and for noise stimuli, 40 dB.(ABSTRACT TRUNCATED AT 400 WORDS)     

Temporally selective processing of communication signals by auditory midbrain neurons

Perception of the temporal structure of acoustic signals contributes critically to vocal signaling. In the aquatic clawed frog Xenopus laevis, calls differ primarily in the temporal parameter of click rate, which conveys sexual identity and reproductive state. We show here that an ensemble of auditory neurons in the laminar nucleus of the torus semicircularis (TS) of X. laevis specializes in encoding vocalization click rates. We recorded single TS units while pure tones, natural calls, and synthetic clicks were presented directly to the tympanum via a vibration-stimulation probe. Synthesized click rates ranged from 4 to 50 Hz, the rate at which the clicks begin to overlap. Frequency selectivity and temporal processing were characterized using response-intensity curves, temporal-discharge patterns, and autocorrelations of reduplicated responses to click trains. Characteristic frequencies ranged from 140 to 3,250 Hz, with minimum thresholds of -90 dB re 1 mm/s at 500 Hz and -76 dB at 1,100 Hz near the dominant frequency of female clicks. Unlike units in the auditory nerve and dorsal medullary nucleus, most toral units respond selectively to the behaviorally relevant temporal feature of the rate of clicks in calls. The majority of neurons (85%) were selective for click rates, and this selectivity remained unchanged over sound levels 10 to 20 dB above threshold. Selective neurons give phasic, tonic, or adapting responses to tone bursts and click trains. Some algorithms that could compute temporally selective receptive fields are described.     

Cortisol Effects on Attentional Processes in Man as Indicated by Event-Related Potentials

Glacocorticoids which are secreted from the adrenal cortex, particularly in response to stressful stimuli, are assumed to influence brain functions related to stimulus perception and processing. To determine underlying mechanisms of this action the present study investigated the effects of physiologically enhanced plasma glucocurticoid levels on auditory event-related potentials (AERPs) reflecting different aspects of stimulus processing. Sixteen male adult subjects were tested in a dichotic listening paradigm containing four types of tone pips: standard and deviant target pips, which the subject either had to attend to, or to ignore. AERPs to the tone pips provided measures of different perceptual and attentional processes. Subjects were tested in a double-blind fashion according to a within-subject cross-over design under either 16 mg hydrocortisone, infused over the experimental period of 1 hrs, or placebo. Compared to placebo sessions, under cortisol treatment a slightly decreased amplitude of the N1 component was obtained independently of the type of tone pip presented. In addition, mismatch negativity, measured as the difference amplitude between AERP waveforms to standard and deviant target pips in the unattended ear, was substantially reduced by hydrocortisone. Results support an inhibitory action of enhanced plasma cortisol levels on stimulus processing mediated by the nonspecific sensory system.     

Synaptic events and discharge patterns of cochlear nucleus cells. I. Steady-frequency tone bursts.

Unitary discharge patterns (peristimulus time histograms or PSTH) and synaptic events were studies with intracellular recording techniques in 164 cat cochlear nucleus cells to steady-frequency tone bursts 250 ms in duration. There were four response types defined on the basis of the shape of the discharge patterns to tones at the characteristic or best frequency. Primarylike units resemble eighth nerve fibres and have a maximum discharge at tone onset, followed by a smooth decline to a steady level of activity. Buildup units have a transient response at tone onset, followed a period of little or not activity before gradually increasing their discharge rate for the remainder of the tone burst. Onset units have an initial burst of spikes at the onset, with little or no activity for the remainder of the tone burst. Pause units have a long latency (10-30 ms) between tone onset and the appearance of low levels of unit activity, which then gradually increase in rate for the remainder of the tone burst. Changes in signal frequency or intensity within the excitatory response area did not modify response patterns of primarylike and onset units, but could evoke primarylike patterns in buildup and pause units. Inhibition manifested by suppression of spontaneous activity and membrane hyperpolarization were of three kinds: 1) in response to signals at the edges of the excitatory response area (i.e., the inhibitory surround) and detected in onset buildup, and pause units but not in primarylike units; 2) occurring at the offset of tones in the excitatory response area and detected in all four types of cochlear nucleus cells; 3) during excitatory tone bursts in onset and buildup units associated with the periods of suppressed unit activity. Membrane hyperpolarization did not accompany the delay in unit activity after tone onset in pause units. Inhibitory events in cochlear nucleus cells provide mechanisms for producing diversity in the temporal pattern of discharges to acoustic signals which may underly the encoding of complex features of sounds.     

Statistical analysis and interpretation of the initial response of cochlear nucleus neurons to tone bursts

1. Subject of investigation is the initial response of cochlear nucleus neurons and units presumed to be auditory nerve fibres to CF tone burst stimulation. 2. The initial response is characterized by computing the distribution of the latency of the first spike and of the duration of the first interval in the ensemble of responses to a large number of stimuli. 3. In many of the neurons the properties of both distributions appear to be related. The presumed auditory nerve fibres and spontaneously active cochlear nucleus neurons showing only activation responses to tonal stimuli (A type) exhibit irregularity in both response onset and intervals. Minimum latency and minimum first intervals are short. On the other hand, spontaneously active neurons with both activation and suppression in the response area (AS type) and silent neurons showing only activation (A(S) type) often show a more precisely timed onset of response and narrow interval distributions. In many neurons this leads to oscillations in the PSTH (chopping). In these neurons minimum latency and minimum first interval have higher values. The longer minimum latency cannot be attribute-d to longer pure time delays in these neurons. 4. The results are interpreted as speaking in favour of temporal integration as an important mechanism in many of the AS and A(S) neurons, particularly those in the DCN. The firing patterns of A neurons are thought to indicate virtual absence of this mechanism. 5. Using pure time delay estimates derived from cross-correlation functions, computed from the responses to stationary noise, an attempt is made to estimate the integration time in the cochlear and in the cochlear nucleus neurons.