Duration-selective Neurons Research Articles

Object size determines the spatial spread of visual time.

A key question for temporal processing research is how the nervous system extracts event duration, despite a notable lack of neural structures dedicated to duration encoding. This is in stark contrast with the orderly arrangement of neurons tasked with spatial processing. In this study, we examine the linkage between the spatial and temporal domains. We use sensory adaptation techniques to generate after-effects where perceived duration is either compressed or expanded in the opposite direction to the adapting stimulus' duration. Our results indicate that these after-effects are broadly tuned, extending over an area approximately five times the size of the stimulus. This region is directly related to the size of the adapting stimulus—the larger the adapting stimulus the greater the spatial spread of the after-effect. We construct a simple model to test predictions based on overlapping adapted versus non-adapted neuronal populations and show that our effects cannot be explained by any single, fixed-scale neural filtering. Rather, our effects are best explained by a self-scaled mechanism underpinned by duration selective neurons that also pool spatial information across earlier stages of visual processing.

Echo amplitude selectivity of the bat is better for expected than for unexpected echo duration

A previous study shows that most inferior collicular neurons of the bat discharge maximally to a best duration and these duration-selective neurons have better echo frequency selectivity when the duration of both echo and pulse matches the best duration. In this study, we show that these duration-selective collicular neurons also have the sharpest echo amplitude selectivity when the duration of both echo and pulse matches the best duration. These data indicate that bats can better extract multiple parameters of expected than unexpected echo within the same time window after pulse emission. These data also support the previous studies showing that bats prepare their auditory system to analyze expected returning echoes within a time window after pulse emission.

Duration selectivity of neurons in the inferior colliculus of the FM bat, miniopterus magnate determined under different pulse repetition rate

Duration selectivity of neurons in the inferior colliculus of the FM bat, miniopterus magnate determined under different pulse repetition rate

The recovery cycle of bat duration-selective collicular neurons varies with hunting phase

During hunting, duration selectivity and recovery cycle underlie a bat's ability to determine echo duration and target distance (echo ranging). This study shows that the recovery cycle of most duration-selective neurons in the bat central nucleus of the inferior colliculus neurons varies with biologically relevant pulse-echo (P-E) duration and amplitude. As such, neurons with short best duration recover rapidly when stimulated with P-E pairs with short duration and small P-E amplitude difference, whereas neurons with long best duration recover rapidly when stimulated with P-E pairs with long duration and large P-E amplitude difference. These data indicate that different groups of duration-selective neurons underlie the bat's ability to effectively perform echo recognition and ranging during different phases of hunting.

Midbrain Auditory Neurons Integrate Excitation and Inhibition to Generate Duration Selectivity: AnIn VivoWhole-Cell Patch Study in Anurans

Sound duration can play a pivotal role in the reproductive behavior of anuran amphibians. Here, we report the first whole-cell recordings from duration-selective neurons in the anuran torus semicircularis, in vivo. We show that most short-pass duration-selective cells exhibited short-latency inhibition and delayed excitation. The duration of the inhibition increased with tone burst duration. Hence, for long-duration tone bursts, inhibition overlapped with excitation, reducing or eliminating spikes; no postinhibitory rebound was present. Other short-pass cells, however, showed inhibition only for long-duration tone bursts. Bandpass duration selectivity also involved interplay between inhibition and excitation; inhibition negated excitation with tone bursts that exceeded the optimum duration. Additionally, however, bandpass selectivity arose from stimulus-dependent excitation; tone bursts of sufficiently long duration were required to elicit excitation. Similarly, long-pass neurons showed inhibition and duration-dependent enhancement of excitation; long-pass selectivity resulted from enhanced excitation outlasting the transient inhibition or, in some cases, excitation overriding concurrent inhibition. Last, we evaluated the stimulus specificity of duration-selective neurons to variations in pulse repetition rate. We show that (1) most neurons that exhibited long-pass selectivity for tone-burst duration nonetheless responded to short-duration pulses when repeated at particular rates, and (2) some neurons that showed selectivity for tone burst duration also showed selectivity for pulse train duration. These novel response profiles appear to result from interplay between inhibition and time- and activity-dependent changes in excitation strength. These findings are discussed in the context of prevailing models of duration selectivity and acoustic communication in anurans.

Bat inferior collicular neurons have the greatest frequency selectivity when determined with best-duration pulses

During hunting, insectivorous bats such as Eptesicus fuscus progressively increase the pulse repetition rate, shorten the pulse duration, and lower the frequency and amplitude of emitted pulses as they search, approach and finally intercept insects or negotiate obstacles. As such, analysis of an echo parameter by the bat is inevitably affected by other co-varying echo parameters. The present study examined the effect of pulse duration on frequency selectivity of neurons in the central nucleus of the inferior colliculus (IC) of the big brown bat. A family of iso-level frequency tuning curves of each IC neuron was first measured with tone bursts of different durations. The bandwidth of iso-level frequency tuning curves within each family was then compared. Our data show that most IC neurons discharge maximally to a particular pulse duration which is defined as the best duration (BDu). The iso-level frequency tuning curves of these duration-selective neurons have the narrowest bandwidth when measured with the BDu pulse than with non-BDu pulses. They also have the narrowest bandwidth when measured with a short than with a long BDu pulse. These data suggest that frequency selectivity of duration-selective IC neurons becomes sharper when short echo duration at the final phase of hunting is encoded by IC neurons that have short BDu.

GABA-mediated echo duration selectivity of inferior collicular neurons of Eptesicus fuscus, determined with single pulses and pulse–echo pairs

When insectivorous bats such as Eptesicus fuscus emit ultrasonic signals and analyze the returning echoes to hunt insects, duration selectivity of auditory neurons plays an important role in echo recognition. The success of prey capture indicates that they can effectively encode progressively shortened echo duration throughout the hunting process. The present study examines the echo duration selectivity of neurons in the central nucleus of the bat inferior colliculus (IC) under stimulation conditions of single pulses and pulse-echo (P-E) pairs. This study also examines the role of gamma-aminobutyric acid (GABA)ergic inhibition in shaping echo duration selectivity of IC neurons. The data obtained show that the echo duration selectivity of IC neurons is sharper when determined with P-E pairs than with single pulses. Echo duration selectivity also sharpens with shortening of pulse duration and P-E gap. Bicuculline application decreases and GABA application increases echo duration selectivity of IC neurons. The degree of change in echo duration selectivity progressively increases with shortening of pulse duration and P-E gap during bicuculline application while the opposite is observed during the GABA application. These data indicate that the GABAergic inhibition contributes to sharpening of echo duration selectivity of IC neurons and facilitates echo recognition by bats throughout different phases of hunting.

The role of GABAergic inhibition in shaping duration selectivity of bat inferior collicular neurons determined with temporally patterned sound trains

A previous study has shown that duration selectivity of neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus becomes sharper with increasing pulse repetition rate (PRR). The present study examines the role of GABAergic inhibition in improving duration selectivity of bat IC neurons with PRR by means of iontophoretic application of GABA as well as its antagonist, bicuculline. Duration selectivity of IC neurons is studied by plotting the duration tuning curves with the number of impulses per pulse against the pulse duration. Duration tuning curves of IC neurons are described as band-, short-, long- and all-pass in terms of filtering properties to sound duration. Bicuculline application produces more pronounced broadening of duration tuning curves at high than at low PRR. Conversely, GABA application produces more pronounced narrowing of duration tuning curves at low than at high PRR. In either case, sharpening of duration selectivity of IC neurons with increasing PRR is abolished during drug application. The duration tuning curves of IC neurons progressively broadens with recording depth. Broadening of duration tuning curves during bicuculline application is more pronounced for neurons at upper than at deep IC. This progressive decrease in duration selectivity with recording depth is discussed in relation to spatial distribution gradient of GABA A receptors in the IC. Possible biological significance of these findings relevant to bat echolocation is discussed.

Duration Selective Neurons in the Inferior Colliculus of the Rat: Topographic Distribution and Relation of Duration Sensitivity to Other Response Properties

Many animals use duration to help them identify the source and meaning of a sound. Duration-sensitive neurons have been found in the auditory midbrain of mammals and amphibians, where their selectivity seems to correspond to the lengths of species-specific vocalizations. In this study, single neurons in the rat inferior colliculus (IC) were tested for sensitivity to sound duration. About one-half (54%) of the units sampled showed some form of duration selectivity. The majority of these (76%) were long-pass neurons that responded to sounds exceeding some duration threshold (range: 5-60 ms). Band-pass neurons, which only responded to a restricted range of durations, made up 13% of duration-sensitive neurons (best durations: 15-120 ms). Other units displayed short-pass (2%) or mixed (9%) response patterns. The majority of duration-sensitive neurons were localized outside the central nucleus of the IC, especially in the dorsal cortex, where more than one-half of the neurons sampled had long-pass selectivity for duration. Band-pass duration tuned neurons were only found outside the central nucleus. Characteristics of duration-sensitive neurons in the rat support the idea that this filtering arises through an interaction of excitatory and inhibitory inputs that converge in the IC. Band-pass neurons typically responded at sound offset, suggesting that their tuning is created through the same mechanisms that have been described in echolocating bats. The finding that the first-spike latencies of all long-pass neurons were longer than the shortest duration to which they responded supports the idea that they receive transient inhibition before, or simultaneously with, a sustained excitatory input. The ranges of selectivity in rat IC neurons are within the range of durations of rat vocalizations. These data suggest that a population of neurons in the rat IC have evolved to transmit information about behaviorally relevant sound durations using mechanisms that are common to all mammals, with an emphasis on long-pass tuning characteristics.

Duration Selectivity of Neurons in the Inferior Colliculus of the Big Brown Bat: Tolerance to Changes in Sound Level

At and above the level of the inferior colliculus (IC), some neurons respond maximally to a limited range of sound durations, with little or no excitatory response to durations outside of this range. Such neurons have been termed "duration tuned" or "duration selective." In this study we examined the effects of varying signal amplitude on best duration, width of tuning, and first spike latency of duration tuned neurons in the IC of the big brown bat, Eptesicus fuscus. Response areas as a function of stimulus duration and intensity took a variety of forms, including open (V-shaped), narrow and level tolerant (U-shaped), or closed (O-shaped). The majority (82%) of duration tuned neurons had narrow U-shaped or O-shaped duration response areas. Those with narrow U-shaped response areas retained their duration tuning across a broad dynamic range, < or = 50 dB above threshold, whereas those with O-shaped response areas were narrowly tuned to both stimulus duration and amplitude. For about one-half (55%) of the neurons with either a U- or O-shaped response areas, best duration (BD) changed by <1 ms across the range of suprathreshold amplitudes tested. Changes in BD most often took the form of a shift to slightly shorter durations as stimulus level increased. For the majority (65%) of U- and O-shaped neurons, 50% width of duration tuning changed by <2 ms with increasing amplitude. Latency of response at BD remained stable across changes in sound level, suggesting that the relative strengths of excitatory and inhibitory inputs to duration tuned neurons remain in balance over a wide dynamic range of sound pressure levels.

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

The inferior colliculus (IC) is the first place in the central auditory pathway where duration-selective neurons are found. Previous neuropharmacological and electrophysiological studies have shown that they are created there and have led to a conceptual model in which excitatory and inhibitory inputs are offset in time so that the cell fires only when sound duration is such that onset- and offset-evoked excitation coincide; the response is suppressed by inhibition at other durations. We tested predictions from the model using paired tone stimulation and extracellular recording in the IC of the big brown bat, Eptesicus fuscus. Responses to a best duration (BD) tone were used as a probe to examine the strength and time course of inhibition activated by a nonexcitatory (NE) tone of the same frequency but differing in duration. As the relative time between the BD and NE tones was varied, the activity evoked by the BD tone was affected in ways comparable with backward, simultaneous, and forward masking. Responses to the BD tone were completely suppressed at short interstimulus intervals when the BD tone preceded the NE tone. Suppression was also seen when the stimuli temporally overlapped and summed and at intervals when the BD tone followed the NE tone. The results show that duration-selective neurons receive an onset-evoked, inhibitory input that precedes their excitatory input. The period of leading inhibition was correlated with BD and first spike latency. The results suggest how inhibition in the CNS could explain temporal masking phenomena, including backward masking.

Neural Representation of Sound Duration in the Inferior Colliculus of the Mouse

In this study we examined the neuronal responses of single units to different sound durations in the inferior colliculus (IC) of the mouse. One hundred and one recorded units were classified into onset (58%), sustained (9%), on-sustained (22%), pauser (9%) and chopper (2%) response patterns. Thirty-four percent of the recorded units showing stronger responses to long stimulus durations were defined as long-duration-selective neurons. Twenty-five percent of the units preferred a narrow range of sound durations and were classified as band-pass neurons. Ten percent of the units responded preferentially to short stimulus durations and thus displayed short-duration selectivity. Twelve percent of the units that responded with nearly constant spike counts to stimuli of varying duration were classified as all-pass neurons. In contrast to the result of no short-duration-selective neurons found in chinchilla IC, we observed that some of the onset units in the IC of the mouse displayed a short duration preference. The best duration range of the duration-selective neurons in the present study corresponds to the duration range of mouse calls. We suggest that an inhibitory mechanism contributes to the duration selectivity observed in the present study.

Sound duration selectivity in the pallid bat inferior colliculus

Neurons selective for sound duration have been reported in the auditory midbrain and cortex of several specialized vertebrate species that process behaviorally relevant signals of stereotypic duration. This study examines duration selectivity in the inferior colliculus (IC) of the pallid bat to determine if this selectivity is limited to regions that serve echolocation, or if it extends to low-frequency regions that serve passive listening. It also focuses on the temporal response properties of duration-selective neurons to elucidate mechanisms that may underlie the creation of this selectivity. Of 140 neurons tested, 36% were selective for short durations of ≤7 ms, and acted as short-pass or bandpass duration filters. Sixteen percent, termed long duration neurons, differed in that they required minimum sound durations of 5–50 ms before responding, and all acted as long-pass duration filters. Short duration neurons were equally common in the high-frequency region serving echolocation and the lateral low-frequency region that serves passive listening, indicating that selectivity for short duration sounds was not associated only with the specialized function of echolocation. Long duration neurons were most common in the medial low-frequency region IC. Selectivity for short and long duration sounds was therefore not uniformly distributed across the IC. Analyses of the temporal response properties of short duration neurons, and the application of bicuculline to block γ-aminobutyric acid-A receptors, were used to infer the synaptic interactions that underlie the creation of duration selectivity, the role of inhibition in its creation, and whether a coincidence mechanism proposed by Casseday et al. (Science 264 (1994) 847–850) is consistent with the behavior of the duration-selective neurons recorded in the pallid bat IC. Present results suggest that while some neurons do behave in a manner that is consistent with the coincidence mechanism, the behaviors of others suggest that more than one mechanism may create a selectivity for short duration sounds.

Long-latency neurons in auditory cortex involved in temporal integration: theoretical analysis of experimental data

A previous experimental study (He et al., 1997) found 132 duration-selective neurons with long latencies of greater than 30 ms in the dorsal zone of cat auditory cortex. The mechanism by which such long-latency neurons integrate information during their latent period is investigated by analysis of the temporal relationship between the stimulus and neuronal response. In the present study, we developed a one-layer perceptron to examine the above temporal relationship of the experimental results. The acoustic stimulus was represented as a contiguous series of sequential short time epochs. The perceptron was trained by using the spike data as the desired outputs and the acoustic stimuli (in digital format) as the inputs. The adaptive weights between the outputs and the inputs after training indicated the temporal relationship between neuronal responses and the stimuli. The contribution of each time epoch of the stimulus could be either positive or negative: the positive contribution corresponds to excitatory input and the negative contribution to inhibitory input. Long-duration-selective neurons were found to receive mainly excitatory input along the entire effective stimulus duration. However, duration-tuned neurons received excitatory input for only the time period from the stimulus onset to their best durations, and inhibitory thereafter. The temporal integration pattern of short-duration-selective neurons was similar to duration-tuned neurons. However, short-duration-selective neurons received excitatory input only at the beginning of the stimulus. Each of the duration-threshold neurons integrated auditory information only for a restricted time period of the stimulus, suggesting that they have a time window over the stimulus time domain. Non-duration-threshold neurons have time windows extending from the stimulus onset onward. The assembly of duration-threshold neurons and non-duration-threshold neurons may collectively represent the time axis of the stimulus.

Temporal Integration and Duration Tuning in the Dorsal Zone of Cat Auditory Cortex

The present study examined auditory cortical neurons, the responses of which depended on the duration of noise bursts. We recorded from 150 neurons with response latencies exceeding 30 msec and from 28 neurons with OFF responses to auditory stimuli in the dorsal zone of cat auditory cortex. Of 150 long-latency neurons, 132 displayed some form of duration selectivity. Seventy-eight were classified as selective for long durations. Among the long-duration-selective neurons, 30 responded only to noise burst stimuli with durations longer than a minimal threshold and were classified further as duration threshold neurons. Of 132 duration-selective neurons, 41 responded selectively to noise bursts of short duration; 13 showed maximal responses to noise bursts of a particular duration and could be regarded as duration-tuned neurons. OFF-response neurons included ones that were long-duration-selective, duration-tuned, and nonduration-selective. Duration tuning has been described previously only at the midbrain level in amphibians and bats. The present finding of sensitivity to sound duration in at least one region of cat auditory cortex indicates that this form of neural tuning may be important for hearing in all vertebrates, and for processing of sound at multiple levels in the auditory pathway. The duration tuning in the cat auditory cortex was much broader, and the best duration was distributed over a wider range than in the bat inferior colliculus. We suggest that the duration selectivity of the long-latency neurons results from integration along the time domain of a stimulus during the latent period.