A temporal hierarchy for conspecific vocalization discrimination in humans.

Introduction: Discrimination of species-specific vocalizations is fundamental for survival and social interactions. Its unique behavioral relevance has encouraged the identification of circumscribed brain regions exhibiting selective responses (Belin et al., 2004), while the role of network dynamics has received less attention. Those studies that have examined the brain dynamics of vocalization discrimination leave unresolved the timing and the inter-relationship between general categorization, attention, and speech-related processes (Levy et al., 2001, 2003; Charest et al., 2009). Given these discrepancies and the presence of several confounding factors, electrical neuroimaging analyses were applied to auditory evoked-potential (AEPs) to acoustically and psychophysically controlled non-verbal human and animal vocalizations. This revealed which region(s) exhibit voice-sensitive responses and in which sequence. Methods: Subjects (N=10) performed a living vs. man-made 'oddball' auditory discrimination task, such that on a given block of trials 'target' stimuli occurred 10% of the time. Stimuli were complex, meaningful sounds of 500ms duration. There were 120 different sound files in total, 60 of which represented sounds of living objects and 60 man-made objects. The stimuli that were the focus of the present investigation were restricted to those of living objects within blocks where no response was required. These stimuli were further sorted between human non-verbal vocalizations and animal vocalizations. They were also controlled in terms of their spectrograms and formant distributions. Continuous 64-channel EEG was acquired through Neuroscan Synamps referenced to the nose, band-pass filtered 0.05-200Hz, and digitized at 1000Hz. Peri-stimulus epochs of continuous EEG (-100ms to 900ms) were visually inspected for artifacts, 40Hz low-passed filtered and baseline corrected using the pre-stimulus period . Averages were computed from each subject separately. AEPs in response to animal and human vocalizations were analyzed with respect to differences of Global Field Power (GFP) and with respect to changes of the voltage configurations at the scalp (reviewed in Murray et al., 2008). The former provides a measure of the strength of the electric field irrespective of topographic differences; the latter identifies changes in spatial configurations of the underlying sources independently of the response strength. In addition, we utilized the local auto-regressive average distributed linear inverse solution (LAURA; Grave de Peralta Menendez et al., 2001) to visualize and statistically contrast the likely underlying sources of effects identified in the preceding analysis steps. Results: We found differential activity in response to human vocalizations over three periods in the post-stimulus interval, and this response was always stronger than that to animal vocalizations. The first differential response (169-219ms) was a consequence of a modulation in strength of a common brain network localized into the right superior temporal sulcus (STS; Brodmann's Area (BA) 22) and extending into the superior temporal gyrus (STG; BA 41). A second difference (291-357ms) also followed from strength modulations of a common network with statistical differences localized to the left inferior precentral and prefrontal gyrus (BA 6/45). These two first strength modulations correlated (Spearman's rho(8)=0.770; p=0.009) indicative of functional coupling between temporally segregated stages of vocalization discrimination. A third difference (389-667ms) followed from strength and topographic modulations and was localized to the left superior frontal gyrus (BA10) although this third difference did not reach our spatial criterion of 12 continuous voxels. Conclusions: We show that voice discrimination unfolds over multiple temporal stages, involving a wide network of brain regions. The initial stages of vocalization discrimination are based on modulations in response strength within a common brain network with no evidence for a voice-selective module. The latency of this effect parallels that of face discrimination (Bentin et al., 2007), supporting the possibility that voice and face processes can mutually inform one another. Putative underlying sources (localized in the right STS; BA 22) are consistent with prior hemodynamic imaging evidence in humans (Belin et al., 2004). Our effect over the 291-357ms post-stimulus period overlaps the 'voice-specific-response' reported by Levy et al. (Levy et al., 2001) and the estimated underlying sources (left BA6/45) were in agreement with previous findings in humans (Fecteau et al., 2005). These results challenge the idea that circumscribed and selective areas subserve con-specific vocalization processing.

Vocalization of the shrew Suncus etruscus and Crocidura during normothermia and torpor

The vocalization of the shrews Suncus etruscus and Crocidura russula during normothermia and torpor is investigated. While frequency and call duration are independent of body temperature, the tremolo structure shows a spreading correlated with falling body temperature. The particular calls emitted during torpor are defence calls, modified by merely physiological factors. Their main function might be of intraspecific nature

A temporal hierarchy for conspecific vocalization discrimination in humans.

The ability to discriminate conspecific vocalizations is observed across species and early during development. However, its neurophysiologic mechanism remains controversial, particularly regarding whether it involves specialized processes with dedicated neural machinery. We identified spatiotemporal brain mechanisms for conspecific vocalization discrimination in humans by applying electrical neuroimaging analyses to auditory evoked potentials (AEPs) in response to acoustically and psychophysically controlled nonverbal human and animal vocalizations as well as sounds of man-made objects. AEP strength modulations in the absence of topographic modulations are suggestive of statistically indistinguishable brain networks. First, responses were significantly stronger, but topographically indistinguishable to human versus animal vocalizations starting at 169-219 ms after stimulus onset and within regions of the right superior temporal sulcus and superior temporal gyrus. This effect correlated with another AEP strength modulation occurring at 291-357 ms that was localized within the left inferior prefrontal and precentral gyri. Temporally segregated and spatially distributed stages of vocalization discrimination are thus functionally coupled and demonstrate how conventional views of functional specialization must incorporate network dynamics. Second, vocalization discrimination is not subject to facilitated processing in time, but instead lags more general categorization by approximately 100 ms, indicative of hierarchical processing during object discrimination. Third, although differences between human and animal vocalizations persisted when analyses were performed at a single-object level or extended to include additional (man-made) sound categories, at no latency were responses to human vocalizations stronger than those to all other categories. Vocalization discrimination transpires at times synchronous with that of face discrimination but is not functionally specialized.

Robust discrimination between EEG responses to categories of environmental sounds in early coma.

Humans can recognize categories of environmental sounds, including vocalizations produced by humans and animals and the sounds of man-made objects. Most neuroimaging investigations of environmental sound discrimination have studied subjects while consciously perceiving and often explicitly recognizing the stimuli. Consequently, it remains unclear to what extent auditory object processing occurs independently of task demands and consciousness. Studies in animal models have shown that environmental sound discrimination at a neural level persists even in anesthetized preparations, whereas data from anesthetized humans has thus far provided null results. Here, we studied comatose patients as a model of environmental sound discrimination capacities during unconsciousness. We included 19 comatose patients treated with therapeutic hypothermia (TH) during the first 2 days of coma, while recording nineteen-channel electroencephalography (EEG). At the level of each individual patient, we applied a decoding algorithm to quantify the differential EEG responses to human vs. animal vocalizations as well as to sounds of living vocalizations vs. man-made objects. Discrimination between vocalization types was accurate in 11 patients and discrimination between sounds from living and man-made sources in 10 patients. At the group level, the results were significant only for the comparison between vocalization types. These results lay the groundwork for disentangling truly preferential activations in response to auditory categories, and the contribution of awareness to auditory category discrimination.

Post-traumatic mutism in children: clinical characteristics, pattern of recovery and clinicopathological correlations.

Among the numerous clinical syndromes observed after severe traumatic head injury, post-traumatic mutism is a disorder rarely reported in adults and not studied in any detail in children. We report seven children between the ages of 3 1/2 and 14 years who sustained severe head injury and developed post-traumatic mutism. We aim to give a precise clinical characterization of this disorder, discuss differential diagnosis and correlations with brain imaging and suggest its probable neurological substrate. After a coma lasting from 5 to 25 days, the seven patients who suffered from post-traumatic mutism went through a period of total absence of verbal production lasting from 5 to 94 days, associated with the recovery of non-verbal communication skills and emotional vocalization. During the first days after the recovery of speech, all patients were able to produce correct small sentences with a hypophonic and monotonous voice, moderate dysarthria, word finding difficulties but no signs of aphasia, and preserved oral comprehension. The neurological signs in the acute phase (III nerve paresis in three of seven patients, signs of autonomic dysfunctions in five of seven patients), the results of the brain imaging and the experimental animal data all suggest the involvement of mesencephalic structures as playing a key role in the aetiology of post-traumatic mutism.

Condition-dependent genetic benefits of extrapair fertilization in female blue tits Cyanistes caeruleus.

In many socially monogamous birds, both partners perform extrapair copulations (EPC). As this behaviour potentially inflicts direct costs on females, they are currently hypothesized to search for genetic benefits for descendants, either as 'good' or 'complementary' genes. Although these hypotheses have found some support, several studies failed to find any beneficial consequence of EPC, and whether this behaviour is adaptive to females is subject to discussion. Here, we test these two hypotheses in a natural population of blue tits by accounting for the effect of most parameters known to potentially affect extrapair fertilization. Results suggest that female body mass affected the type of extrapair genetic benefits obtained. Heavy females obtained extrapair fertilizations when their social male was of low quality (as reflected by sexual display) and produced larger extrapair than within-pair chicks. Lean females obtained extrapair fertilizations when their social mate was genetically similar, thereby producing more heterozygous extrapair chicks. Our results suggest that mating patterns may be condition-dependent.

Individual vocal signatures in barn owl nestlings: does individual recognition have an adaptive role in sibling vocal competition?

To compete over limited parental resources, young animals communicate with their parents and siblings by producing honest vocal signals of need. Components of begging calls that are sensitive to food deprivation may honestly signal need, whereas other components may be associated with individual-specific attributes that do not change with time such as identity, sex, absolute age and hierarchy. In a sib-sib communication system where barn owl (Tyto alba) nestlings vocally negotiate priority access to food resources, we show that calls have individual signatures that are used by nestlings to recognize which siblings are motivated to compete, even if most vocalization features vary with hunger level. Nestlings were more identifiable when food-deprived than food-satiated, suggesting that vocal identity is emphasized when the benefit of winning a vocal contest is higher. In broods where siblings interact iteratively, we speculate that individual-specific signature permits siblings to verify that the most vocal individual in the absence of parents is the one that indeed perceived the food brought by parents. Individual recognition may also allow nestlings to associate identity with individual-specific characteristics such as position in the within-brood dominance hierarchy. Calls indeed revealed age hierarchy and to a lower extent sex and absolute age. Using a cross-fostering experimental design, we show that most acoustic features were related to the nest of origin (but not the nest of rearing), suggesting a genetic or an early developmental effect on the ontogeny of vocal signatures. To conclude, our study suggests that sibling competition has promoted the evolution of vocal behaviours that signal not only hunger level but also intrinsic individual characteristics such as identity, family, sex and age.

Effects of hatching asynchrony on sibling negotiation, begging, jostling for position and within-brood food allocation in the barn owl Tyto alba

When siblings differ markedly in their need for food, they may benefit from signalling to each other their willingness to contest the next indivisible food item delivered by the parents. This sib-sib communication system, referred to as 'sibling negotiation', may allow them to adjust optimally to investment in begging. Using barn owl (Two alba) broods. I assessed the role of within-brood age hierarchy on sibling negotiation, and in turn on jostling for position where parents predictably deliver food (i.e. nest-box entrance), begging and within-brood food allocation. More specifically, I examined three predictions derived from a game-theoretical model of sibling negotiation where a senior and a junior sibling compete for food resources (Roulin, 2002a, Johnstone and Roulin, 2003): (1) begging effort invested by the senior sibling should be less sensitive to the junior sibling's negotiation than vice versa; (2) the junior should invest less effort in sibling negotiation than its senior sibling but a similar amount of effort in begging; and (3) within-brood food allocation should be directly related to begging but only indirectly to sibling negotiation. Two-chick broods were created and vocalization in the absence (negotiation signals directed to siblings) and presence (begging signals directed to parents) of parents was recorded. In support of the first prediction, juniors begged at a low cadence after their senior sibling negotiated intensely, probably because negotiation reflects prospective investment in begging and hence willingness to compete. In contrast, the begging of senior siblings was not sensitive to their junior sibling's negotiation. In contrast to the second prediction, juniors negotiated and begged more intensely than their senior sibling apparently because they were hungrier rather than younger. In line with the third prediction, juniors monopolized food delivered by their parents when their senior sibling begged at a low level. The begging cadence of both the junior and senior sibling, the junior's negotiation cadence, the difference in age between the two nest-mates and jostling for position were not associated with the likelihood of monopolizing food. In conclusion, sibling negotiation appears to influence begging behaviour, which, in turn, affects within-brood food allocation. Juniors may negotiate to challenge their senior siblings, and thereby determine whether seniors are less hungry before deciding to beg for food. In contrast, seniors may negotiate to deter juniors from begging.

Indicators used by clinicians to assess pain in the brain injured

INTRODUCTION. The assessment of pain in critically ill brain-injured patients is challenging for health professionals. In addition to be unable to self-report, the confused and stereotyped behaviors of these patients are likely to alter their ''normal'' pain responses. Therefore, the pain indicators observed in the general critically ill population may not be appropriate. OBJECTIVES. To identify behavioral and physiological indicators used by clinicians to assess pain in critically ill brain-injured patients who are unable to self-report. METHODS.Amixed-method design was used with the first step being the combination of the results of an integrative literature review with the results of nominal groups of 12 nurses and four physicians. The second step involved a web-based survey to establish content validity. Fourteen experts (clinicians and academics) from three French speaking European countries rated the relevance of each indicator. A content validity index (CVI) was computed for each indicator (I-CVI) and for each category (S-CVI). RESULTS. The first step generated 52 indicators. These indicators were classified into six categories: facial expressions, position/movement, muscle tension, vocalization, compliance with ventilator, and physiological indicators. In the second step, the agreement between raters was high with an Intraclass Correlation Coefficient of 0.88 (95% CI 0.83-0.92). The I-CVIs ranged from 0.07 to 1. Indicators with an I-CVI below 0.5 (n = 12) were not retained, resulting in a final list of 30 indicators. The CVI for this final list was 0.75 with categories ranging from 0.67 (compliance with ventilation) to 0.87 (vocalization). CONCLUSIONS. This process identified specific pain indicators for critically ill braininjured patients. Further evaluation is in progress to test the validity and relevance of these indicators in the clinical setting.

Vocal sib-sib interactions: how siblings adjust signaling level to each other

Game theory states that iterative interactions between individuals are necessary to adjust behaviour optimally to one another. Although our understanding of the role of begging signals in the resolution of parent-offspring conflict over parental investment rests on game theory implying repeated interactions between family members, empiricists usually consider interactions at the exact moment when parents allocate food among the brood. Therefore, the mechanisms by which siblings adjust signalling level to one another remain unclear. We tackled this issue in the barn owl, Tyto alba. In the absence of parents, hungry nestlings signal vocally to siblings their intention to contest vigorously the next, indivisible, food item. Such behaviour deters siblings from competing and begging when parents return to the nest. In experimental two-chick broods, nestlings producing the longest calls in the absence of parents, a signal of hunger level, were more successful at monopolizing the food item at the first parental feeding visit of the night. Moreover, nestlings increased (versus decreased) call duration when their sibling produced longer (versus shorter) calls, and an individual was more likely to call again if its sibling began to vocalize before or just after it had ended its previous call. These results are in agreement with the hypothesis that siblings challenge each other vocally to reinforce the honesty of sib-sib communication and to resolve conflicts over which individual will have priority of access to the next delivered food item. Siblings challenge each other vocally to confirm that the level of signalling accurately reflects motivation.

Accuracy of plant assemblage predictions from species distribution models varies along environmental gradients

Aim: Climatic niche modelling of species and community distributions implicitly assumes strong and constant climatic determinism across geographic space. This assumption had however never been tested so far. We tested it by assessing how stacked-species distribution models (S-SDMs) perform for predicting plant species assemblages along elevation. Location: Western Swiss Alps. Methods: Using robust presence-absence data, we first assessed the ability of topo-climatic S-SDMs to predict plant assemblages in a study area encompassing a 2800 m wide elevation gradient. We then assessed the relationships among several evaluation metrics and trait-based tests of community assembly rules. Results: The standard errors of individual SDMs decreased significantly towards higher elevations. Overall, the S-SDM overpredicted far more than they underpredicted richness and could not reproduce the humpback curve along elevation. Overprediction was greater at low and mid-range elevations in absolute values but greater at high elevations when standardised by the actual richness. Looking at species composition, the evaluation metrics accounting for both the presence and absence of species (overall prediction success and kappa) or focusing on correctly predicted absences (specificity) increased with increasing elevation, while the metrics focusing on correctly predicted presences (Jaccard index and sensitivity) decreased. The best overall evaluation - as driven by specificity - occurred at high elevation where species assemblages were shown to be under significant environmental filtering of small plants. In contrast, the decreased overall accuracy in the lowlands was associated with functional patterns representing any type of assembly rule (environmental filtering, limiting similarity or null assembly). Main Conclusions: Our study reveals interesting patterns of change in S-SDM errors with changes in assembly rules along elevation. Yet, significant levels of assemblage prediction errors occurred throughout the gradient, calling for further improvement of SDMs, e.g., by adding key environmental filters that act at fine scales and developing approaches to account for variations in the influence of predictors along environmental gradients.

Information retention during competitive interactions : siblings need to constantly repeat vocal displays

Memory is essential to adjust behaviour according to past experience. In societies where animals interact on numerous occasions, memory of previous social interactions may help optimise investment in competition. How long information about the resource holding potential and motivation to compete of conspecifics is retained depends on how fast the value of this information fades, but also on the cost and benefit of retaining information. Information retention has never been investigated in the context of interactions prevailing within the family and more specifically sibling competition. In the absence of parents, barn owl (Tyto alba) nestlings vocally compete for priority of access to the next indivisible food item brought by a parent. The finding that owlets eavesdrop on vocal interactions between siblings to adjust investment in vocalization once competing with them suggests that they memorize siblings' vocal interactions. Playback experiments showed that owlets take into account the past siblings' vocal performance that signals hunger for at least 15 min, but only if the performance was witnessed during a sufficiently long period of time (30 min). Moreover, using natural vocal exchanges in another set of individuals, we showed that sibling signalling was no more taken into account after a few minutes. This suggests that young barn owls need to continuously display their motivation to trigger siblings' withdrawal from the current competition. Repeating a vocal display may ensure its honesty. Studying the extent to which individuals retain past information is important to understand how individuals adjust their competitive investment over resources.

Efficiency and significance of multiple vocal signals in sibling competition

Animals can compete for resources by displaying various acoustic signals that may differentially affect the outcome of competition. We propose the hypothesis that the most efficient signal to deter opponents should be the one that most honestly reveals motivation to compete. We tested this hypothesis in the barn owl (Tyto alba) in which nestlings produce more calls of longer duration than siblings to compete for priority access to the indivisible prey item their parents will deliver next. Because nestlings increase call rate to a larger extent than call duration when they become hungrier, call rate would signal more accurately hunger level. This leads us to propose three predictions. First, a high number of calls should be more efficient in deterring siblings to compete than long calls. Second, the rate at which an individual calls should be more sensitive to variation in the intensity of the sibling vocal competition than the duration of its calls. Third, call rate should influence competitors' vocalization for a longer period of time than call duration. To test these three predictions we performed playback experiments by broadcasting to singleton nestlings calls of varying durations and at different rates. According to the first prediction, singleton nestlings became less vocal to a larger extent when we broadcasted more calls compared to longer calls. In line with the second prediction, nestlings reduced vocalization rate to a larger extent than call duration when we broadcasted more or longer calls. Finally, call rate had a longer influence on opponent's vocal behavior than call duration. Young animals thus actively and differentially use multiple signaling components to compete with their siblings over parental resources.

From bird to sparrow: Learning-induced modulations in fine-grained semantic discrimination.

Recognition of environmental sounds is believed to proceed through discrimination steps from broad to more narrow categories. Very little is known about the neural processes that underlie fine-grained discrimination within narrow categories or about their plasticity in relation to newly acquired expertise. We investigated how the cortical representation of birdsongs is modulated by brief training to recognize individual species. During a 60-minute session, participants learned to recognize a set of birdsongs; they improved significantly their performance for trained (T) but not control species (C), which were counterbalanced across participants. Auditory evoked potentials (AEPs) were recorded during pre- and post-training sessions. Pre vs. post changes in AEPs were significantly different between T and C i) at 206-232ms post stimulus onset within a cluster on the anterior part of the left superior temporal gyrus; ii) at 246-291ms in the left middle frontal gyrus; and iii) 512-545ms in the left middle temporal gyrus as well as bilaterally in the cingulate cortex. All effects were driven by weaker activity for T than C species. Thus, expertise in discriminating T species modulated early stages of semantic processing, during and immediately after the time window that sustains the discrimination between human vs. animal vocalizations. Moreover, the training-induced plasticity is reflected by the sharpening of a left lateralized semantic network, including the anterior part of the temporal convexity and the frontal cortex. Training to identify birdsongs influenced, however, also the processing of C species, but at a much later stage. Correct discrimination of untrained sounds seems to require an additional step which results from lower-level features analysis such as apperception. We therefore suggest that the access to objects within an auditory semantic category is different and depends on subject's level of expertise. More specifically, correct intra-categorical auditory discrimination for untrained items follows the temporal hierarchy and transpires in a late stage of semantic processing. On the other hand, correct categorization of individually trained stimuli occurs earlier, during a period contemporaneous with human vs. animal vocalization discrimination, and involves a parallel semantic pathway requiring expertise.