Species identity and the temporal characteristics of fish acoustic signals

Analyses of the acoustic signals of fish show that fine-scale temporal patterns of signals are what vary among species. A growing body of research addressing the topic of species differences in fish acoustic signals suggests that these differences are related to mate choice or species isolation. However, little behavioral work has been done to determine whether these temporal differences are actually used in discriminating conspecific sounds from interspecific sounds. In this article, the authors review three cases--Centrachids, Mormyrids, and Pomancentrids--for which species specificity in both signal production and differential response to acoustic signals have been demonstrated. Work done on damselfish (Dascyllus albisella) is an especially good example and thus may serve as a model for future work.     

Hemispheric differences in temporal resolution

A review of the relevant clinical and experimental literature gives the conclusion that the cerebral hemispheres differ in temporal resolution of input, with the language-dominant hemisphere showing finer acuity. This conclusion is supported by evidence from performance of patients with unilateral brain damage on tests of temporal resolution, performance of developmental dyslexics on similar tasks, and left-right sensory field differences in temporal acuity in normal human subjects. While it is unlikely that a hemispheric difference in temporal resolution is sufficient to give a complete account of lateralized functions, such attempts to show more primitive physiological differences between the hemispheres are more likely to be fruitful than attempts which differentiate the hemispheres in terms of higher-order psychological functions.     

Time, rate, and conditioning

The authors draw together and develop previous timing models for a broad range of conditioning phenomena to reveal their common conceptual foundations: First, conditioning depends on the learning of the temporal intervals between events and the reciprocals of these intervals, the rates of event occurrence. Second, remembered intervals and rates translate into observed behavior through decision processes whose structure is adapted to noise in the decision variables. The noise and the uncertainties consequent on it have both subjective and objective origins. A third feature of these models is their timescale invariance, which the authors argue is a very important property evident in the available experimental data. This conceptual framework is similar to the psychophysical conceptual framework in which contemporary models of sensory processing are rooted. The authors contrast it with the associative conceptual framework.     

Turning the attentional blink on and off: Opposing effects of spatial and temporal noise

Brain oscillations in various frequency bands have been shown to be an important means of enabling interarea communication for high-level cognitive performance. Interestingly, perturbation to such oscillations in the form of weak noise has been shown to benefit perception in tasks such as the attentional blink (AB). Here, we investigated perturbation intrinsic to the AB task in two conditions in which noise arose from either temporal or spatial discontinuity. Consistent with theoretical predictions, temporal discontinuity resulted in a reduced AB, whereas spatial discontinuity resulted in an increased AB. The results are discussed in the framework of both stochastic resonance theory and pretarget alpha oscillations, two neurally based accounts of perceptual processing.     

Binaural and temporal integration of the loudness of tones and noises

Subjects judged the loudness of tones (Experiment 1) and of bursts of noise (Experiment 2) that varied in intensity and duration as well as in mode of presentation (monaural vs. binaural). Both monaural and binaural loudness, for both types of signals, obeyed the bilinear-interaction prediction of the classic temporal integration model. The loudness of short tones grows as a power function of both intensity and duration with different exponents for the two factors (.2 and .3, respectively). The loudness of wide-band noises grows as a power function of duration (with an exponent of approximately .6) but not of sound pressure. For tones, binaural summation was constant but fell short of full additivity. For noises, summation changed across level and duration. Temporal summation followed the same course for monaural and binaural tonal stimuli but not for noise stimuli. Notwithstanding these differences between tone and noise, we concluded that binaural and temporal summation are independently operating integrative networks within the auditory system. The usefulness of establishing the underlying metric structure for temporal summation is emphasized.     

Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

Persistent, bidirectional changes in synaptic signaling (that is, potentiation and depression of the synapse) can be induced by the precise timing of individual pre- and postsynaptic action potentials. However, far less attention has been paid to the ability of paired trains of action potentials to elicit persistent potentiation or depression. We examined plasticity following the pairing of spike trains in the touch mechanosensory neuron (T cell) and S interneuron (S cell) in the medicinal leech. Long-term potentiation (LTP) of T to S signaling was elicited when the T-cell spike train preceded the S-cell train. An interval 0 to +1 sec between the T- and S-cell spike trains was required to elicit long-term potentiation (LTP), and this potentiation was NMDA receptor (NMDAR)-dependent. Long-term depression (LTD) was elicited when S-cell activity preceded T-cell activity and the interval between the two spike trains was -0.2 sec to -10 sec. This surprisingly broad temporal window involved two distinct cellular mechanisms; an NMDAR-mediated LTD (NMDAR-LTD) when the pairing interval was relatively brief (<-1 sec) and an endocannabinoid-mediated LTD (eCB-LTD) when longer pairing intervals were used (-1 to -10 sec). This eCB-LTD also required activation of a presynaptic transient receptor potential vanilloid (TRPV)-like receptor, presynaptic Ca(2+) release from intracellular stores and activation of voltage-gated Ca(2+) channels (VGCCs). These findings demonstrate that the pairing of spike trains elicits timing-dependent forms of LTP and LTD that are supported by a complex set of cellular mechanisms involving NMDARs and endocannabinoid activation of TRPV-like receptors.     

Hemispheric asymmetries for temporal information processing: transient detection versus sustained monitoring

This study investigated functional differences in the processing of visual temporal information between the left and right hemispheres (LH and RH). Participants indicated whether or not a checkerboard pattern contained a temporal gap lasting between 10 and 40 ms. When the stimulus contained a temporal signal (i.e. a gap), responses were more accurate for the right visual field-left hemisphere (RVF-LH) than for the left visual field-right hemisphere (LVF-RH). This RVF-LH advantage was larger for the shorter gap durations (Experiments 1 and 2), suggesting that the LH has finer temporal resolution than the RH, and is efficient for transient detection. In contrast, for noise trials (i.e. trial without temporal signals), there was a LVF-RH advantage. This LVF-RH advantage was observed when the entire stimulus duration was long (240 ms, Experiment 1), but was eliminated when the duration was short (120 ms, Experiment 2). In Experiment 3, where the gap was placed toward the end of the stimulus presentation, a LVF-RH advantage was found for noise trials whereas the RVF-LH advantage was eliminated for signal trials. It is likely that participants needed to monitor the stimulus for a longer period of time when the gap was absent (i.e. noise trials) or was placed toward the end of the presentation. The RH may therefore be more efficient in the sustained monitoring of visual temporal information whereas the LH is more efficient for transient detection.     

Ear advantages for temporal resolution in baboons

On the assumption that temporal resolution underlies an individual's ear advantage for speech perception, one would predict an ear advantage for a temporal resolution task to correlate precisely with an ear advantage for the discrimination of consonant-vowel syllables that differ in their temporal features. A gap detection task that required the resolution of brief silent intervals in bursts of noise was employed to test this hypothesis in four baboons. The findings offer support for such a hypothesis and thus increase the feasibility of an animal model of functional asymmetry in the auditory system.     

Objective assessment of the functional role of spike train correlations using information measures

The functional role of correlations between neuronal spike trains remains strongly debated. This debate partly stems from the lack of a standardized analysis technique capable of accurately quantifying the role of correlations in stimulus encoding. We believe that information theoretic measures may represent an objective method for analysing the functional role of neuronal correlations. Here we show that information analysis of pairs of spike trains allows the information content present in the firing rate to be disambiguated from any extra information that may be present in the temporal relationships of the two spike trains. We validate and illustrate the method by applying it to simulated data with variable degrees of known synchrony, and by applying it to recordings from pairs of sites in the primary visual cortex of anaesthetized cats. We discuss the importance of information theoretic analysis in elucidating the neuronal mechanisms underlying object identification.     

Temporal ventriloquism in a purely temporal context

This study examines how audiovisual signals are combined in time for a temporal analogue of the ventriloquist effect in a purely temporal context, that is, no spatial grounding of signals or other spatial facilitation. Observers were presented with two successive intervals, each defined by a 1250-ms tone, and indicated in which interval a brief audiovisual stimulus (visual flash + noise burst) occurred later. In "test" intervals, the audiovisual stimulus was presented with a small asynchrony, while in "probe" intervals it was synchronous and presented at various times guided by an adaptive staircase to find the perceived temporal location of the asynchronous stimulus. As in spatial ventriloquism, and consistent with maximum likelihood estimation (MLE), the asynchronous audiovisual signal was shifted toward the more reliably localized component (audition, for all observers). Moreover, these temporal shifts could be forward or backward in time, depending on the asynchrony order, suggesting perceived timing is not entirely determined by physical timing. However, the critical signature of MLE combination--better bimodal than unimodal precision--was not found. Regardless of the underlying model, these results demonstrate temporal ventriloquism in a paradigm that is defined in a purely temporal context.     

Temporal preparation improves temporal resolution: Evidence from constant foreperiods

Recent research shows that temporal preparation within a constant foreperiod design improves the spatial resolution of visual perception. The present experiments were designed to investigate whether similar benefits of temporal preparation can be observed in a task that requires high temporal resolution. In three experiments, we assessed the effect of temporal preparation on temporal order judgments (TOJs). In Experiment 1, short foreperiods facilitated TOJ for two spatially adjacent dots. This finding was replicated in Experiment 2, in which the temporal order of two spatially overlapping stimuli (“+” and “x”) had to be discriminated. Experiment 3 investigated the time course of temporal preparation by extending these findings to a wide range of different foreperiod durations. The present findings corroborate recent evidence for a perceptual locus of temporal preparation. Most importantly, they show that temporal preparation within a constant foreperiod design improves the temporal resolution of visual perception, independently of whether TOJ requires a decision about the location or about the identity of the target stimuli.     

The temporal weighting of loudness: effects of the level profile

In four experiments, we studied the influence of the level profile of time-varying sounds on temporal perceptual weights for loudness. The sounds consisted of contiguous wideband noise segments on which independent random-level perturbations were imposed. Experiment 1 showed that in sounds with a flat level profile, the first segment receives the highest weight (primacy effect). If, however, a gradual increase in level (fade-in) was imposed on the first few segments, the temporal weights showed a delayed primacy effect: The first unattenuated segment received the highest weight, while the fade-in segments were virtually ignored. This pattern argues against a capture of attention to the onset as the origin of the primacy effect. Experiment 2 demonstrated that listeners adjust their temporal weights to the level profile on a trial-by-trial basis. Experiment 3 ruled out potentially inferior intensity resolution at lower levels as the cause of the delayed primacy effect. Experiment 4 showed that the weighting patterns cannot be explained by perceptual segmentation of the sounds into a variable and a stable part. The results are interpreted in terms of memory and attention processes. We demonstrate that the prediction of loudness can be improved significantly by allowing for nonuniform temporal weights.     

Transient spatial attention degrades temporal resolution

To better understand the interplay between the temporal and spatial components of visual perception, we studied the effects of transient spatial attention on temporal resolution. Given that spatial attention sharpens spatial resolution, can it also affect temporal resolution? To assess temporal resolution, we measured the two-flash fusion threshold When two flashes of light are presented successively to the same location, the two-flash fusion threshold is the minimal interval between the flashes at which they are still perceived as two flashes, rather than a single flash. This assessment of temporal resolution was combined with peripheral precuing--a direct manipulation of transient spatial attention. This allowed us to demonstrate, for the first time, that spatial attention can indeed affect temporal resolution. However, in contrast to its effect on spatial resolution, spatial attention degrades temporal resolution. Two attentional mechanisms that could account for both attentional effects--enhanced spatial resolution and reduced temporal resolution--are discussed.     

Coping with a changing soundscape: avoidance,adjustments and adaptations

Since the industrial age, background anthropogenic noise has become a pervasive feature of many habitable environments. This relatively recent environmental feature can be particularly challenging for organisms that use acoustic forms of communication due to its propensity for masking and decreasing the potential acoustic space of signals. Furthermore, anthropogenic noise may affect biological processes including animal interactions, physiological and behavioural responses to stimuli and cognitive development. However, animals’ cognitive abilities may enable them to cope with high levels of anthropogenic noise through learning, the employment of acoustic and behavioural flexibility as well as the use of multi-modal sensory systems. We are only just beginning to understand how neural structures, endocrine systems and behaviour are mechanistically linked in these scenarios, providing us with information we can use to mitigate deleterious effects of pervasive noise on wildlife, along with highlighting the remarkable adaptability of animals to an increasingly anthropogenic world. In this review, I will focus mainly on birds, due to the amount of literature on the topic, and survey recent advancements made in two main spheres: (1) how anthropogenic noise affects cognitive processes and (2) how cognition enables animals to cope with increasingly noisy environments. I will be highlighting current gaps in our knowledge, such as how noise might impact behavioural traits such as predation, as well as how noise causes physical damage to neurotransmitters and affects stress levels, in order to direct future studies on this topic.     

Near-term fetuses process temporal features of speech

The perception of speech and music requires processing of variations in spectra and amplitude over different time intervals. Near-term fetuses can discriminate acoustic features, such as frequencies and spectra, but whether they can process complex auditory streams, such as speech sequences and more specifically their temporal variations, fast or relatively slow acoustic variations, is unclear. We recorded the cardiac activity of 82 near-term fetuses (38 weeks GA) in quiet sleep during a silent control condition and four 15 s streams presented at 90 dB SPL Leq: two piano melodies with opposite contours, a natural Icelandic sentence and a chimera of the sentence--all its spectral information was replaced with broadband noise, leaving its specific temporal variations in amplitude intact without any phonological information. All stimuli elicited a heart rate deceleration. The response patterns to the melodies were the same and differed significantly from those observed with the Icelandic sentence and its chimera, which did not differ. The melodies elicited a monophasic heart rate deceleration, indicating a stimulus orienting reflex while the Icelandic and its chimera evoked a sustained lower magnitude response, indicating a sustained attentional response or more focused information processing. A conservative interpretation of the data is that near-term fetuses can perceive sound streams and the rapid temporal variations in amplitude that are specific to speech sounds with no spectral variations at all.     

Avoidance learning facilitates temporal processing in the primary auditory cortex

The primary auditory cortex is now known to be involved in learning and memory, as well as auditory perception. For example, spectral tuning often shifts toward or to the frequency of the conditioned stimulus during associative learning. As previous research has focused on tonal frequency, less is known about how learning might alter temporal parameters of response in the auditory cortex. This study addressed the effects of learning on the fidelity of temporal processing. Adult male rats were trained to avoid shock that was signaled by an 8.0 kHz tone. A novel control group received non-contingent tone and shock with shock probability decreasing over days to match the reduced number of shocks received by the avoidance group as they mastered the task. An untrained (nai ve) group served as a baseline. Following training, neuronal responses to white noise and a broad spectrum of tones were determined across the primary auditory cortex in a terminal experiment with subjects under general anesthesia. Avoidance conditioning significantly improved the precision of spike-timing: the coefficient of variation of 1st spike latency was significantly reduced in avoidance animals compared to controls and nai ves, both for tones and for noise. Additionally, avoidance learning was accompanied by a reduction of the latency of peak response, by 2.0-2.5 ms relative to nai ves and approximately 1.0 ms relative to controls. The shock-matched controls also exhibited significantly shorter peak latency of response than nai ves, demonstrating the importance of this non-avoidance control. Plasticity of temporal processing showed no evidence of frequency specificity and developed independently of the non-temporal parameters magnitude of response, frequency tuning and neural threshold, none of which were facilitated. The facilitation of temporal processing suggests that avoidance learning may increase synaptic strength either within the auditory cortex, in the subcortical auditory system, or both.     

Effect of lateralized gaps in noise on the cutaneous blink reflex in humans

The early (R1) and late (R2) components of the cutaneous blink reflex in right-handed humans were recorded in three experiments to examine the lateral symmetry of a simple excitatory process in their brainstem pathways and of the control of the excitability of the pathways by gaps in acoustic noise. Experiment 1 showed that a stimulus below R1-elicitation threshold increased the excitability of the right R1 pathway more than the left but that the rate of decay was similar on both sides. Experiment 2 showed that a brief unilateral gap in noise affected the R1 and R2 reflex pathways bilaterally. Experiment 3 showed that R2 varied with gap duration and that gaps to the left and right ears had indistinguishable effects. The finer temporal resolution of events in the right sensory field of right-handers seen in psychophysical judgments is not seen in the descending control of brainstem excitability.     

Perception of distance calls by budgerigars (Melopsittacus undulatus) and zebra finches (Poephila guttata): assessing species-specific advantages

Budgerigars (Melopsittacus undulatus) and zebra finches (Poephila guttata) share a common functional class of vocalizations called distance calls. The perception of species-specific distance calls by both species was measured with a habituation-dishabituation operant paradigm. Changes in discrimination performance were noted as listening conditions were modified or stimulus properties were altered. Both species showed better performance for calls of their own species. For zebra finches this tendency increased slightly when a background noise was added to the testing environment. Shifting the frequency region of the calls affected the discrimination performance of male budgerigars but not females or zebra finches. Reversing the temporal order of the calls affected the perceptual advantage for conspecific vocalizations in zebra finches but not in budgerigars. These results highlight species differences in perceiving acoustic communication signals.     

Agonistic screams in wild chimpanzees (Pan troglodytes schweinfurthii) vary as a function of social role

Some nonhuman primates have demonstrated the capacity to communicate about external objects or events, suggesting primate vocalizations can function as referential signals. However, there is little convincing evidence for functionally referential communication in any great ape species. Here, the authors demonstrate that wild chimpanzees (Pan troglodytes schweinfurthii) of Budongo forest, Uganda, give acoustically distinct screams during agonistic interactions depending on the role they play in a conflict. The authors analyzed the acoustic structure of screams of 14 individuals, in the role of both aggressor and victim. The authors found consistent differences in the acoustic structure of the screams, across individuals, depending on the social role the individual played during the conflict. The authors propose that these 2 distinct scream variants, produced by victims and aggressors during agonistic interactions, may be promising candidates for functioning as referential signals.     

Acoustic communication in crocodilians: information encoding and species specificity of juvenile calls

In the Crocodylia order, all species are known for their ability to produce sounds in several communication contexts. Though recent experimental studies have brought evidence of the important biological role of young crocodilian calls, especially at hatching time, the juvenile vocal repertoire still needs to be clarified in order to describe thoroughly the crocodilian acoustic communication channel. The goal of this study is to investigate the acoustic features (structure and information coding) in the contact call of juveniles from three different species (Nile crocodile Crocodylus niloticus, Black caiman, Melanosuchus niger and Spectacled caiman, Caiman crocodilus). We have shown that even though substantial structural differences exist between the calls of different species, they do not seem relevant for crocodilians. Indeed, juveniles and adults from the species studied use a similar and non-species-specific way of encoding information, which relies on frequency modulation parameters. Interestingly, using conditioning experiments, we demonstrated that this tolerance in responses to signals of different acoustic structures was unlikely to be related to a lack of discriminatory abilities. This result reinforced the idea that crocodilians have developed adaptations to use sounds efficiently for communication needs.