Response Properties Of Auditory Neurons Research Articles

Modified synaptic dynamics predict neural activity patterns in an auditory field within the frontal cortex

Frontal areas of the mammalian cortex are thought to be important for cognitive control and complex behaviour. These areas have been studied mostly in humans, non-human primates and rodents. In this article, we present a quantitative characterization of response properties of a frontal auditory area responsive to sound in the brain of Carollia perspicillata, the frontal auditory field (FAF). Bats are highly vocal animals, and they constitute an important experimental model for studying the auditory system. We combined electrophysiology experiments and computational simulations to compare the response properties of auditory neurons found in the bat FAF and auditory cortex (AC) to simple sounds (pure tones). Anatomical studies have shown that the latter provides feedforward inputs to the former. Our results show that bat FAF neurons are responsive to sounds, and however, when compared to AC neurons, they presented sparser, less precise spiking and longer-lasting responses. Based on the results of an integrate-and-fire neuronal model, we suggest that slow, subthreshold, synaptic dynamics can account for the activity pattern of neurons in the FAF. These properties reflect the general function of the frontal cortex and likely result from its connections with multiple brain regions, including cortico-cortical projections from the AC to the FAF.

Incorporating Midbrain Adaptation to Mean Sound Level Improves Models of Auditory Cortical Processing.

An ability to accurately predict how sensory neurons respond to novel stimuli is critical if we are to fully characterize their response properties. Attempts to model these responses have had a distinguished history, but it has proven difficult to improve their predictive power significantly beyond that of simple, mostly linear receptive field models. Here we show that auditory cortex receptive field models benefit from a nonlinear preprocessing stage that replicates known adaptation properties of the auditory midbrain. This improves their predictive power across a wide range of stimuli but keeps model complexity low as it introduces no new free parameters. Incorporating the adaptive coding properties of neurons will likely improve receptive field models in other sensory modalities too.

Auditory response properties of neurons in the putamen and globus pallidus of awake cats

Several decades of research have provided evidence that the basal ganglia are closely involved in motor processes. Recent clinical, electrophysiological, behavioral data have revealed that the basal ganglia also receive afferent input from the auditory system, but the detailed auditory response characteristics have not yet reported. The present study aimed to reveal the acoustic response properties of neurons in parts of the basal ganglia. We recorded single-unit activities from the putamen (PU) and globus pallidus (GP) of awake cats passively listening to pure tones, click trains, and natural sounds. Our major findings were: 1) responses in both PU and GP neurons were elicited by pure-tone stimuli, whereas PU neurons had lower intensity thresholds, shorter response latencies, shorter excitatory duration, and larger response magnitudes than GP neurons. 2) Some GP neurons showed a suppressive response lasting throughout the stimulus period. 3) Both PU and GP did not follow periodically repeated click stimuli well, and most neurons only showed a phasic response at the stimulus onset and offset. 4) In response to natural sounds, PU also showed a stronger magnitude and shorter duration of excitatory response than GP. The selectivity for natural sounds was low in both nuclei. 5) Nonbiological environmental sounds more efficiently evoked responses in PU and GP than the vocalizations of conspecifics and other species. Our results provide insights into how acoustic signals are processed in the basal ganglia and revealed the distinction of PU and GP in sensory representation.

Moderate noise induced cognition impairment of mice and its underlying mechanisms

Noise pollution is recognized as a serious human health problem in modern society. The aim of the present study was to explore the effects of moderate-intensity white noise exposure on learning and memory of mice, and the underlying mechanisms. The learning and memory ability of mice were evaluated by water maze and step-down inhibitory avoidance experiments respectively, following 1, 3, and 6weeks noise exposure (80dB SPL, 2h/day). To explore potential mechanisms, we determined levels of oxidative stress in the inferior colliculus (IC), auditory cortex (AC), and hippocampus (the structures comprising the critical encephalic region associated with the acoustic lemniscal ascending pathway), the phosphorylation of microtubule-associated protein tau in the hippocampus (important role in learning and memory), and the basic auditory response properties of neurons in the IC. Moderate-intensity noise exposure impaired the learning and memory ability of mice in both water maze and step-down inhibitory avoidance experiments, and the longer the noise exposure time the greater the impairment. At 6weeks after noise exposure, there was also evidence of oxidative damage in the IC, AC, and hippocampus, hyperphosphorylated tau protein in the hippocampus, and significant changes in the auditory response properties of neurons in the IC. These data results suggest that moderate-intensity noise can progressively impair the learning and memory ability of mice, which may result from peroxidative damage, tau hyperphosphorylation, and auditory coding alteration.

Encoding properties of auditory neurons in the brain of a soniferous damselfish: response to simple tones and complex conspecific signals

The fish auditory system encodes important acoustic stimuli used in social communication, but few studies have examined response properties of central auditory neurons to natural signals. We determined the features and responses of single hindbrain and midbrain auditory neurons to tone bursts and playbacks of conspecific sounds in the soniferous damselfish, Abudefduf abdominalis. Most auditory neurons were either silent or had slow irregular resting discharge rates <20 spikes s(-1). Average best frequency for neurons to tone stimuli was approximately 130 Hz but ranged from 80 to 400 Hz with strong phase-locking. This low-frequency sensitivity matches the frequency band of natural sounds. Auditory neurons were also modulated by playbacks of conspecific sounds with thresholds similar to 100 Hz tones, but these thresholds were lower than that of tones at other test frequencies. Thresholds of neurons to natural sounds were lower in the midbrain than the hindbrain. This is the first study to compare response properties of auditory neurons to both simple tones and complex stimuli in the brain of a recently derived soniferous perciform that lacks accessory auditory structures. These data demonstrate that the auditory fish brain is most sensitive to the frequency and temporal components of natural pulsed sounds that provide important signals for conspecific communication.

Auditory response properties of neurons in the tectal longitudinal column of the rat

The newly-discovered tectal longitudinal column (TLC) spans the paramedian region of the mammalian tectum. It has connections with several nuclei of the auditory system. In this report, we provide the first detailed description of the responses of TLC neurons to auditory stimuli, including monaural and binaural tones and amplitude modulated tones. For comparison, responses in the inferior colliculus (IC) were also recorded. Neurons in the TLC were sensitive to similar ranges of frequency as IC neurons, could have comparably low thresholds, and showed primarily excitatory responses to stimulation of the contralateral ear with either phasic or sustained response patterns. Differences of TLC compared to IC neurons included broader frequency tuning, higher average threshold, longer response latencies, little synchronization or rate tuning to amplitude modulation frequency and a smaller degree of inhibition evoked by stimulation of the ipsilateral ear. These features of TLC neurons suggest a role for the TLC in descending auditory pathways.

The serotonin releaser fenfluramine alters the auditory responses of inferior colliculus neurons

Local direct application of the neuromodulator serotonin strongly influences auditory response properties of neurons in the inferior colliculus (IC), but endogenous stores of serotonin may be released in a distinct spatial or temporal pattern. To explore this issue, the serotonin releaser fenfluramine was iontophoretically applied to extracellularly recorded neurons in the IC of the Mexican free-tailed bat ( Tadarida brasiliensis). Fenfluramine mimicked the effects of serotonin on spike count and first spike latency in most neurons, and its effects could be blocked by co-application of serotonin receptor antagonists, consistent with fenfluramine-evoked serotonin release. Responses to fenfluramine did not vary during single applications or across multiple applications, suggesting that fenfluramine did not deplete serotonin stores. A predicted gradient in the effects of fenfluramine with serotonin fiber density was not observed, but neurons with fenfluramine-evoked increases in latency occurred at relatively greater recording depths compared to other neurons with similar characteristic frequencies. These findings support the conclusion that there may be spatial differences in the effects of exogenous and endogenous sources of serotonin, but that other factors such as the identities and locations of serotonin receptors are also likely to play a role in determining the dynamics of serotonergic effects.

Long‐term sensorineural hearing loss induces functional changes in the rat auditory nerve

Loss of cochlear hair cells in the rat initiates degenerative change within the primary auditory neurons (ANs) of the cochlea. These degenerative changes include loss of peripheral processes, demyelination and ultimately cell death. This pathology will affect the biophysical processes involved in action potential generation and propagation to an electrical stimulus via a cochlear implant. We measured the response properties of ANs, with particular reference to their refractory behaviour, in normal, short- (9 weeks) and long-term (> 52 weeks) deafened rats. AN loss was moderate in the short-term and severe in the long-term deafened animals. AN activity was elicited using a brief electrical stimulus delivered via a bipolar electrode array implanted into the cochlea. The general response properties of ANs recorded from deafened cochleae were similar to those observed in normal cochleae, i.e. a monotonic increase in the probability of firing and a decrease in response latency and temporal jitter with increasing stimulus intensity. However, the absolute refractory period was significantly prolonged in animals deaf for > 12 months (P = 0.0026). Deafened animals also exhibited a highly significant increase in threshold compared with normal controls (P < 0.001). These functional changes have implications for recipients of cochlear implants and potential therapies directed toward halting or reversing AN pathology.

Monaural middle ear destruction in juvenile and adult mice: effects on responses to sound direction in the inferior colliculus ipsilateral to the intact ear

This study examined the effect of monaural middle ear destruction on auditory responses to sound direction in the inferior colliculus (IC) of the laboratory mice, Mus musculus. Monaural middle ear destruction was performed on juvenile and adult mice (the experimental mice). Auditory response properties of neurons to ipsilateral and contralateral sounds (I-40° and C-40°) were examined in the IC ipsilateral to the intact ear 4 weeks later. IC neurons of control mice had higher minimum thresholds (MTs), larger Q n ( Q 10, Q 30) values but smaller dynamic ranges at I-40° than at C-40°. These direction-dependent response properties were not observed for IC neurons of experimental juvenile and adult mice. However, Q n values of IC neurons were significantly smaller in experimental juvenile than in control and experimental adult mice. Normal tonotopic organization in terms of positive correlation between recording depth and best frequency (BF) was observed in the IC of control and experimental adult mice at both sound directions but not in the IC of experimental juvenile mice. A positive correlation of increasing MT with BF was only observed for IC neurons in control mice but not in both experimental mice. Possible mechanisms for these different response properties are discussed.

Intracellular characterization of suppressive responses in supragranular pyramidal neurons of cat primary auditory cortex in vivo.

Several suppressive processes shape the response properties of auditory neurons, namely lateral inhibition, non-monotonic rate level function and excitation/inhibition binaural interaction. By combining intracellular recording from and staining of layers 2 and 3 pyramidal neurons (PNs) in cat primary auditory cortex, we demonstrate the temporal aspects of depolarization and hyperpolarization underlying these suppressions using pure tone stimulation. Two populations can be distinguished by the occurrence of hyperpolarization following onset depolarization (O-DEP). In layer 2 PNs there is an absence of hyperpolarization following O-DEP, while in layer 3 PNs hyperpolarization follows O-DEP. The latency of O-DEP is shortest at the neuron's best frequency. The latency shortens as sound intensity increases. In non-monotonic PNs, hyperpolarization onset becomes shorter as sound intensity increases. This earlier onset of hyperpolarization shortens the duration of the preceding O-DEP, resulting in a decreased O-DEP amplitude. Diverse patterns in the temporal interaction of depolarization and hyperpolarization underlie the binaural suppression interaction. These results demonstrate that diverse suppressive responses result from differences in the temporal timing of excitation and inhibition. The present results also suggest the possibility of distinct connections between PNs responding in a similar manner.

The effect of monaural middle ear destruction on postnatal development of auditory response properties of mouse inferior collicular neurons

This study examined the effect of monaural middle ear destruction on postnatal development of auditory response properties of inferior collicular (IC) neurons of the laboratory mouse, Mus musculus. Monaural middle ear destruction was performed on juvenile and adult mice and the auditory response properties of neurons in both ICs were examined 4 weeks thereafter. IC neurons of control mice typically had lower minimum thresholds, larger dynamic ranges and greater Q 10 values than IC neurons of experimental juvenile and adult mice. In experimental mice, neurons in the ipsilateral IC (relative to the intact ear) typically had longer latencies, higher minimum thresholds, and smaller dynamic ranges than neurons in the contralateral IC. In experimental adult mice, neurons in the ipsilateral IC had sharper frequency tuning curves than neurons in the contralateral IC. Clear tonotopic organization was only observed in the IC of control mice and experimental adult mice. However, the correlation of increasing minimum threshold with best frequency was observed for IC neurons in control mice but not in experimental juvenile and adult mice. Possible mechanisms for these different response properties are discussed.

Sexually stimulating signals of canary (Serinus canaria) songs: evidence for a female-specific auditory representation in the HVc nucleus during the breeding season.

During the breeding season under long-day conditions, male canaries sing sexually attractive songs and females respond behaviorally to such songs. This study assessed whether auditory response properties of neurons in nucleus HVc of female and male canaries are tuned to sexually salient song features: special song phrases and canary song segmentation. In sexually receptive female canaries, neurons responded to special song phrases with a decreased spike rate and were sensitive to canary song segmentation. The nonreceptive females showed no clear response to special song phrases. In females on short days, neurons responded to song phrases with an increase in activity. In males on long days, they exhibited phasic responses after the phrase onset, whatever the song phrase and song segmentation. This study demonstrates both a plasticity in relation to females' sexual responsiveness and a sexual dimorphism in the auditory processing performed in the HVc.

Response characteristics of neurons in the medial geniculate body of the little brown bat to simple and temporally-patterned sounds.

We examined the auditory response properties of neurons in the medial geniculate body of unanesthetized little brown bats (Myotis lucifugus). The units' selectivities to stimulus frequency, amplitude and duration were not significantly different from those of neurons in the inferior colliculus (Condon et al. 1994), which provides the primary excitatory input to the medial geniculate body, or in the auditory cortex (Condon et al. 1997) which receives primary input from the medial geniculate body. However, in response to trains of unmodulated tone pulses, the upper cutoff frequency for time-locked discharges (64 +/- 46.9 pulses per second or pps) and the mean number of spikes per pulse (19.2 +/- 12.2 pps), were intermediate to those for the inferior colliculus and auditory cortex. Further, in response to amplitude-modulated pulse trains, medial geniculate body units displayed a degree of response facilitation that was intermediate to that of the inferior colliculus and auditory cortex inferior colliculus: 1.32 +/- 0.33; medial geniculate body: 1.75 +/- 0.26; auditory cortex: 2.52 +/- 0.96, P < 0.01). These data suggest that the representation of isolated tone pulses is not significantly altered along the colliculothalamo-cortical axis, but that the fidelity of representation of temporally patterned signals progressively degrades along this axis. The degradation in response fidelity allows the system to better extract the salient feature in complex amplitude-modulated signals.

Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development

Auditory experience is critical for vocal learning in songbirds as in humans. Therefore, in a search for neural mechanisms for song learning and recognition, the auditory response properties of neurons in the anterior forebrain (AF) pathway of the songbird brain were investigated. This pathway plays an essential but poorly understood role during the period of song development when auditory feedback is most crucial. Single-unit recordings demonstrated that both the lateral magnocellular nucleus of the anterior neostriatum (LMAN) and Area X (X) contain auditory neurons in adult male finches. These neurons are strongly selective for both spectral and temporal properties of song; they respond more robustly to the bird's own song (BOS) than to songs of conspecific individuals, and they respond less well to the BOS if it is played in reverse. In addition, X neurons are more broadly responsive than LMAN neurons, suggesting that responses to song become progressively more refined along this pathway. Both X and LMAN of young male finches early in the process of song learning (30-45 d old) also contain song-responsive auditory neurons, but these juvenile neurons lack the song and order selectivity present in adult birds. The spectral and temporal selectivity of the adult AF auditory neurons therefore arises during development in neurons that are initially broadly song-responsive. These neurons provide one of the clearest examples of experience-dependent acquisition of complex stimulus selectivity. Moreover, the auditory properties of the AF circuit suggest that one of its functions may be to mediate the auditory learning and feedback so essential to song development.

Auditory tuning for spatial cues in the barn owl basal ganglia

1. The basal ganglia are known to contribute to spatially guided behavior. In this study, we investigated the auditory response properties of neurons in the barn owl paleostriatum augmentum (PA), the homologue of the mammalian striatum. The data suggest that the barn owl PA is specialized to process spatial cues and, like the mammalian striatum, is involved in spatial behavior. 2. Single- and multiunit sites were recorded extracellularly in ketamine-anesthetized owls. Spatial receptive fields were measured with a free-field sound source, and tuning for frequency and interaural differences in timing (ITD) and level (ILD) was assessed using digitally synthesized dichotic stimuli. 3. Spatial receptive fields measured at nine multiunit sites were tuned to restricted regions of space: tuning widths at half-maximum response averaged 22 +/- 9.6 degrees (mean +/- SD) in azimuth and 54 +/- 22 degrees in elevation. 4. PA sites responded strongly to broadband sounds. When frequency tuning could be measured (n = 145/201 sites), tuning was broad, averaging 2.7 kHz at half-maximum response, and tended to be centered near the high end of the owl's audible range. The mean best frequency was 6.2 kHz. 5. All PA sites (n = 201) were selective for both ITD and ILD. ITD tuning curves typically exhibited a single, large "primary" peak and often smaller, "secondary" peaks at ITDs ipsilateral and/or contralateral to the primary peak. Three indices quantified the selectivity of PA sites for ITD. The first index, which was the percent difference between the minimum and maximum response as a function of ITD, averaged 100 +/- 29%. The second index, which represented the size of the largest secondary peak relative to that of the primary peak, averaged 49 +/- 23%. The third index, which was the width of the primary ITD peak at half-maximum response, averaged only 66 +/- 35 microseconds. 6. The majority (96%; n = 192/201) of PA sites were tuned to a single "best" value of ILD. The widths of ILD tuning curves at half-maximum response averaged 24 +/- 9 dB. 7. On average, sound level had no effect on a site's best ITD or best ILD nor did it affect ITD tuning widths. ILD tuning widths did, however, tend to increase slightly with sound level (average effect was 0.1 dB ILD/dB). 8. Most PA sites responded best to contralateral-ear leading ITDs with a majority being tuned to ITDs near 0 microsecond (corresponding to sound-source locations just contralateral to the midline).(ABSTRACT TRUNCATED AT 400 WORDS)

The untuning of the tuning curve: is it time?

The measures that are currently used to characterize the response properties of auditory neurons, such as tuning curve and Q value, stem primarily from engineering descriptors of electrical circuits. The motivation behind those descriptors in turn derives from the mathematical concepts of Fourier theory and systems (frequency) analysis. It now seems unlikely that the auditory nervous system performs such a frequency analysis and therefore those measures and concept of frequency tuning curves need re-evaluation. It therefore is time that we seriously question the relevance of classical tuning curves for the study of sound communication. The auditory system is uniquely endowed with an ability to process rapid signal variation in time. More attention should be paid to the encoding of temporal waveforms directly in the time domain, rather than invoking a transformation into the frequency domain and the application of mathematical frequency analysis based on engineering principles.

Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc

Song learning shapes the response properties of auditory neurons in the song system to become highly selective for the individual bird's own ("autogenous") song. The auditory representation of autogenous song is achieved in part by neurons that exhibit facilitated responses to combinations of components of song. To understand the circuits that underlie these complex properties, the combination sensitivity of single units in the hyperstriatum ventrale, pars caudale (HVc) of urethane-anesthetized zebra finches was studied. Some neurons exhibited nonlinear temporal summation, spectral summation, or both. The majority of these neurons exhibited low spontaneous rates and phasic responses. Most combination-sensitive neurons required highly accurate copies of sounds derived from the autogenous song and responded weakly to tone bursts, combinations of simple stimuli, or conspecific songs. Temporal combination-sensitive (TCS) neurons required either two or more segments of a single syllable, or two or more syllables of the autogenous song, to elicit a facilitated, excitatory response. TCS neurons integrated auditory input over periods ranging from 80 to 350 msec, although this represents a lower limit. Harmonic combination-sensitive (HCS) neurons required combinations of two harmonics with particular frequency and temporal characteristics that were similar to autogenous song syllables. Both TCS and HCS neurons responded much more weakly when the dynamical spectral features of the autogenous song or syllables were modified than when the dynamical amplitude (waveform) features of the songs were modified. These results suggest that understanding the temporal dynamics of auditory responses in HVc may provide insight into neuronal circuits modified by song learning.

Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum

The lateral amygdaloid nucleus (AL) is anatomically connected with sensory processing structures in the thalamus and cortex and is believed to be critically involved in emotional processing by virtue of these connections. In order to understand further how auditory projections to AL contribute to emotional processing, acoustic response properties of single AL neurons were characterized in rats. Recordings were also made in the posterior striatum dorsal to AL. Many cells in AL and the striatum could be driven by broad-band auditory stimulation with white noise or clicks. Initial onset latencies were typically between 12 and 25 msec. Most cells also had later responses (60-150 msec), and a few only had late responses. In frequency receptive field tests, different classes of cells were identified. One group had relatively clear frequency preferences. Thresholds for these relatively tuned cells tended to be somewhat higher in AL than in the striatum. Frequency preferences for AL cells were always above 10 kHz. Although most striatal cells had preferences for frequencies above 10 kHz, some cells were found with frequencies below 10 kHz as well. A second group of acoustically responsive neurons, much more common in AL than in the striatum, showed no frequency specificity (untuned cells). These responded to a wide range of frequencies, even at intensities near threshold. A third group, found mainly in AL (approximately 60% of the total population of cells examined in AL), exhibited rapid habituation to auditory stimuli. These tended to have high thresholds (80-100 dB). Because these cells habituated so quickly, frequency specificity could not be determined. Responses in AL and the striatum were compared with responses in the "specific" auditory relay nucleus of the thalamus, the ventral division of the medial geniculate body, where cells had shorter onset latencies, narrower tuning functions, and lower-intensity thresholds than cells in AL and striatal areas. These findings show that cells in AL exhibit a wide range of auditory tuning properties and suggest that information processing in the amygdala might be fruitfully studied as a direct extension of processing in sensory afferent structures.

GABAergic inhibition upon auditory response properties of neurons in the dorsal cochlear nucleus of the rat

It is well known that the superficial layers of the dorsal cochlear nucleus (DCN) are rich in GABAergic neurons. We investigated the effects of topical application of GABA receptor agonists and/or antagonists upon the auditory response properties of DCN neurons in rats anesthetized with alpha chloralose-urethane. Auditory stimuli consisted of 20 ms tone bursts presented in a free field. Response properties of DCN neurons were studied before and during iontophoretic application of GABA, bicuculline methiodide (BIC) and muscimol (MUS) alone and GABA with MUS or BIC through triple barrel electrodes glued to the recording microelectrode. Of 68 DCN neurons studied, 27 were sensitive to topical application of the GABA agonists or antagonist. In these neurons, BIC enhanced spontaneous activity as well as auditory responses and decreased the Q-30 quality factor values. MUS reduced auditory responses. BIC often increased the width of the turning curve but GABA and/or MUS reduced it. Without drug application, GABA sensitive neurons tended to have longer response latencies and larger tuning widths at 30 dB above threshold as well as larger Q-30 values as compared with neurons that were insensitive to GABA. These findings suggest that: 1) GABAergic neurons determine the width of the tuning curve in neurons with GABA receptors by curtailing the excitatory response area, and 2) such neurons receive tonic inhibition from intrinsic GABAergic neurons.

Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow

Neuronal activity in the hyperstriatum ventrale, pars caudale (HVc) is associated with and necessary for the production of song by songbirds. HVc neurons also respond to acoustic stimuli. The present investigation assessed the auditory response properties of neurons in HVc by testing with the individual bird's own (autogenous) song and the songs of conspecific birds. Throughout HVc, multiunit clusters preferentially responded to autogenous song. Selectivity for autogenous song was apparent even when compared to similar intradialect songs, and neuronal clusters preferred autogenous song over the (tutor) song model that birds heard during the impressionable phase early in life. The responses to autogenous song were stable in the adult. HVc neurons were sensitive to the acoustic parameters of autogenous song and consistently exhibited a diminished response to modified song. In contrast, field L neurons, which are presumed to be a source of auditory input to HVc, did not exhibit selectivity for autogenous song and showed no special sensitivity to the acoustic parameters of autogenous song. These observations implicate song (motor) learning in shaping the response properties of HVc, but not field L, auditory neurons. It is proposed that HVc auditory neurons may contribute to a bird's ability to discriminate among conspecific songs by acting as an "autogenous reference" during perception of those songs.