Rapid contact call-driven induction of NR2A and NR2B NMDA subunit mRNAs in the auditory thalamus of the budgerigar (Melopsittacus undulatus)

In situ hybridization histochemistry was used to assess the effect of auditory stimulation with natural contact calls on expression of NR2A and NR2B NMDA subunit mRNAs in neurons of the thalamic auditory relay nucleus ovoidalis (Ov) of a vocal learning parrot species, the budgerigar (Melopsittacus undulatus). The results showed that both the core (Ov) and ventromedial shell subdivisions (Ovm) of ovoidalis contained neurons expressing NR2A and NR2B mRNA in no-stimulation control subjects and that the distributions of neurons expressing these subunit mRNAs were very similar in both the core and shell of Ov. Contact call stimulation (5, 30 and 180 min) resulted in substantial increases of 50-60% in the number of neurons expressing NR2A and NR2B mRNAs in both the core and shell. Staining intensity, as measured by the optical density of stained somata approximately doubled compared to controls for both NR2 subunits in the 5 and 30 min conditions, but declined from 30 to 180 min. In all conditions, the density, but not staining intensity, of neurons expressing NR2B exceeded NR2A expression. Furthermore, the density of neurons expressing both subunit mRNAs in call stimulation conditions was greater in the core than in the shell despite the fact that total neuronal density was approximately 20% higher in the shell. Previous experiments have shown that call stimulation is more effective at inducing expression of the immediate early gene zenk in the Ov shell than core; however the present results do not indicate that either NR2A or NR2B mRNA expression mediates this effect since neither subunit exhibits greater expression in Ovm. Ca(++) release is needed for immediate early gene expression, however and, notably, Ovm contains large numbers of neurons containing CGRP, a peptide which has been shown to increase cytosolic Ca(++) levels.     

Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch

Area X, a large sexually dimorphic nucleus in the avian ventral forebrain, is part of a highly discrete system of interconnected nuclei that have been implicated in either song learning or adult song production. Previously, this nucleus has been included in the song system because of its substantial connections with other vocal control nuclei, and because its volume is positively correlated with the capacity for song. In order to directly assess the role of Area X in song behavior, this nucleus was bilaterally lesioned in both juvenile and adult zebra finches, using ibotenic acid. We report here that lesioning Area X disrupts normal song development in juvenile birds, but does not affect the production of stereotyped song by adult birds. Although juvenile-lesioned birds were consistently judged as being in earlier stages of vocal development than age-matched controls, they continued to produce normal song-like vocalizations. Thus, unlike the lateral magnocellular nucleus of the anterior neostriatum, another avian forebrain nucleus implicated in song learning, Area X does not seem to be necessary for sustaining production of juvenile song. Rather, the behavioral results suggest Area X is important for either the acquisition of a song model or the improvement of song through vocal practice.     

Are temporal features crucial acoustic cues in dog vocal recognition?

To investigate the perceptual mechanisms underlying conspecific vocal recognition in canine species, eighteen dogs were presented with playbacks of normal and reversed versions of typical dog vocalizations. Auditory perception was analysed using the head-turn paradigm, a non-invasive technique extensively employed to study hemispheric specializations for processing conspecific vocalizations in primates. The results revealed that dogs usually turn their heads with the right ear leading (left hemisphere activation) in response to the forward version of their typical calls, and with either no bias and the left ear leading (right hemisphere activation) in response to the reversed call versions. Overall, our findings suggest that temporal features are determinant auditory cues for call sound recognition in dogs, and support earlier findings of the role of the left hemisphere in the analyses of intraspecific communication.     

Amino acid release from the intermediate medial hyperstriatum ventrale (IMHV) of day-old chicks following a one-trial passive avoidance task

Indirect evidence has implicated glutamate and gamma-amino butyric acid in memory formation for one-trial passive avoidance learning. We have further examined this by following the time course of glutamate and gamma-amino butyric acid release from slices prepared from the intermediate medial hyperstriatum ventrale of day-old chicks (Ross 1 Chunky) trained to avoid a bead covered in the aversant methylanthranilate. At various times after training, slices of left and right intermediate medial hyperstriatum ventrale were incubated in medium containing 50 mM potassium chloride and amino acid release was determined. Thirty minutes after training there was a bilateral increase in calcium-dependent glutamate release in slices from methylanthranilate-trained chicks compared to those trained to peck water. This increase was sustained until 1 h in the left hyperstriatum when an increase in calcium-dependent gamma-amino butyric acid release was also apparent. Glutamate uptake was also enhanced in left hyperstriatum (30 and 60 min) and in the right at 30 min. In the right intermediate medial hyperstriatum ventrale of methylanthranilate birds glutamate release was increased from 3 to 6.5 h and gamma-amino butyric acid at 6.5 h: a time that corresponded to the mobilization of a late process required if long-term memory was to be formed. These results confirm that the amino acids glutamate and gamma-amino butyric acid are released from the intermediate hyperstriatum ventrale in a calcium-dependent, neurotransmitter-like manner. Furthermore, changes in the release of these two amino acids accompany memory formation for a one-trial learning task in the day-old chick.     

Male vocal competition is dynamic and strongly affected by social contexts in music frogs

Male–male vocal competition in anuran species is critical for mating success; however, it is also highly time-consuming, energetically demanding and likely to increase predation risks. Thus, we hypothesized that changes in the social context would cause male vocal competition to change in real time in order to minimize the costs and maximize the benefits of competition. To test this hypothesis, we assessed the effect of repeating playbacks of either white noise (WN) or male advertisement calls on male call production in the Emei music frog (Babina daunchina), a species in which males build mud-retuse burrows and call from within these nests. Previous studies have shown that calls produced from inside burrows are highly sexually attractive (HSA) to females while those produced outside nests are of low sexual attractiveness (LSA). Results showed that most subjects called responsively after the end of WN playbacks but before the onset of conspecific call stimuli although call numbers were similar, indicating that while males adjusted competitive patterns according to the biological significance of signals, their competitive motivation did not change. Furthermore, these data indicate that the frogs had evolved the ability of interval timing. Moreover, when the inter-stimulus interval (ISI) between playbacks was varied, the subjects preferentially competed with HSA calls when the ISI was short (<4 s) but responded equally to HSA and LSA calls if the ISI was long (≥4 s), suggesting that males allocate competitive efforts depending on both the perceived sexual attractiveness of rivals and the time available for calling. Notably, approximately two-thirds of male calls occurred in response to HSA calls, a preference rate comparable to that previously found for females in phonotaxis experiments and consistent with the idea that the mechanisms underlying both the male’s competitive responses to rivals and the female’s preferences toward potential mates coevolved under the same selective pressure.     

Enlargement of Neuronal Somata in the LMAN Coincides with the Onset of Sensorimotor Learning for Song

The lateral magnocellular nucleus of the anterior neostriatum (LMAN) in the zebra finch (Taeniopygia guttata) has been shown to play a developmentally restricted role that is essential during song-learning processes. Dendritic spine frequencies and synapse numbers in LMAN have been reported to decline in males during early vocal motor learning and thereafter, but not in females, who do not sing. Nissl staining has shown the LMAN volume to be very similar in both sexes, however. To gain more insight into the development of sex-specific differences in LMAN, the size of neuronal somata and cell nuclei were analyzed in 1-μm semithin sections. Cell somata and nuclei were similar in males and females during the initial phases of sensory memory formation for song, but during early vocal motor learning cell size increased in males and decreased in females. Sex differences in neuronal somata size were present at 50 days and remained throughout life. This sex difference may be indicative of a difference in protein biosynthesis in LMAN, arising as a consequence of vocal learning in males.     

Effects of lesions of the central nucleus of the anterior archistriatum on contact call and warble song production in the budgerigar (Melopsittacus undulatus)

We studied the effects of both unilateral and bilateral lesions of the central nucleus of the anterior archistriatum (AAc) on the production of contact calls and warble song in adult male and female budgerigars. Birds were sorted into three experimental groups based on the percentage of AAc destroyed and whether lesions were unilateral or bilateral. The experimental groups were Unilateral Lesion (N = 8), Partial Bilateral Lesion (N = 5), and Bilateral Lesion birds (N = 12). Each group contained both sexes. Unilateral lesions had no demonstrable effects on contact call or warble song production. Bilateral lesions resulted in immediate and permanent disruption of all learned temporal and spectral characteristics of contact calls, although call initiation was not dependent on the AAc. Partial bilateral lesion effects varied with lesion size and location. At least 20-30% sparing of the AAc, including sparing portions of both the dorsal (AAcd) and ventral (AAcv) subdivisions on the same side of the brain, is necessary for production of prelesion contact call patterns. Warble song was absent in birds with complete bilateral destruction. Two birds with large yet incomplete lesions of the AAc sang after surgery, although the warble song of these birds was extremely impoverished and contained only a few of the typical warble song elements. Lesion results indicate that the AAc mediates the production of learned vocal features in male and female budgerigars, with each hemisphere capable of supporting a normal vocal repertoire.     

Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches (Taeniopygia guttata)

Zebra finches communicate via several distinct vocalizations, of which song is the most studied. Behavioral observations indicate that adults are able to discriminate among the songs of different conspecific individuals. In the wild, zebra finches live in structured but mobile colonies, and encounter new individuals on a frequent basis. Thus it seems plausible that adult finches might have the capacity to recognize and remember new songs they encounter on a single day, but this has never been directly tested. Here we devised a simple observational assay to determine whether adult male zebra finches show recognition of a song they have heard repeatedly from taped playbacks, over a single three hour period the day before. We quantified the rate of production of six discrete behaviors (short calls, contact calls, singing, short hops, long hops, and beak swipes) made by adult male zebra finches as they listened to the playbacks. At the onset of song playback, all birds suspended these behaviors and sat silently-occasionally moving their heads. Then, after a measurable period ("response latency"), the birds resumed these activities. We observed that the response latency was long (approximately 10 min) when birds were hearing a particular song for the first time. The response latency was much shorter (approximately 1-2 min) when the birds had heard the same song the day before. Thus, functional song memories must result from as little as 3 h of passive song-exposure. These results suggest that ongoing song learning may play a natural role in the daily life of adult zebra finches, and provide a behavioral reference point for studies of molecular and physiological plasticity in the adult auditory system.     

Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats

A large body of literature implicates the amygdala in Pavlovian fear conditioning. In this study, we examined the contribution of individual amygdaloid nuclei to contextual and auditory fear conditioning in rats. Prior to fear conditioning, rats received a large electrolytic lesion of the amygdala in one hemisphere, and a nucleus-specific neurotoxic lesion in the contralateral hemisphere. Neurotoxic lesions targeted either the lateral nucleus (LA), basolateral and basomedial nuclei (basal nuclei), or central nucleus (CE) of the amygdala. LA and CE lesions attenuated freezing to both contextual and auditory conditional stimuli (CSs). Lesions of the basal nuclei produced deficits in contextual and auditory fear conditioning only when the damage extended into the anterior divisions of the basal nuclei; damage limited to the posterior divisions of the basal nuclei did not significantly impair conditioning to either auditory or contextual CS. These effects were typically not lateralized, although neurotoxic lesions of the posterior divisions of the basal nuclei had greater effects on contextual fear conditioning when the contralateral electrolytic lesion was placed in the right hemisphere. These results indicate that there is significant overlap within the amygdala in the neural pathways mediating fear conditioning to contextual and acoustic CS, and that these forms of learning are not anatomically dissociable at the level of amygdaloid nuclei.     

Mouse vocal communication system: Are ultrasounds learned or innate?

Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.     

Passive avoidance training results in lasting changes in deoxyglucose metabolism in left hemisphere regions of chick brain

Day-old chicks peck when offered a bright bead; if the bead is coated with the bitter-tasting methylanthranilate (M) they avoid it thereafter. 2-[14C] Deoxyglucose injected 1 min prior to training shows increased uptake into the hyperstriatum ventrale (HV) and lobus parolfactorius (LPO) 30 min later compared with control birds which have pecked a water-coated bead (W). To distinguish effects of training from those of consolidation, and to study lateralization of the increased uptake, 2-[14C]deoxyglucose (4 muCi) was injected ip either 5 min before, or 10 or 30 min after training. Thirty minutes after injection, bilateral samples of medial hyperstriatum ventrale (MHV), LPO and palaeostriatum augmentatum (PA)-enriched regions were dissected. Specific radioactivity (dmp/mg X prot) in left and right MHV and left and right LPO was standardized on the mean PA-specific radioactivity for each bird. When 2-DG was injected 5 min prior to training, standardized radioactivity in the left LPO was 26% greater, and in the left MHV 13% greater in M than W birds. There were no differences in the right hemisphere. With injection 10 min after training, there was an increase of 22% in the left LPO of M birds over W, of 29% in the left MHV and 22% in the right MHV. If injection was delayed to 30 min after training, there was no increase in the LPO, but a 13% increase persisted in the left MHV. Enhanced 2DG metabolism following passive avoidance training is thus persistent, lateralized, and, in the MHV at least may represent an aspect of cellular reorganization consequent on experience but independent of the immediate concomitants of training--perhaps part of the process of memory consolidation.     

Development of species identification in ducklings: III. Maturational rectification of perceptual deficit caused by auditory deprivation.

Mute ducklings, devocalized as embryos and maintained in auditory isolation, manifest a selective high-frequency perceptual deficit vis-à-vis the maternal call of their species at 24 hr after hatching. Since it takes a rather specific auditory experiential input to rectify this high-frequency insensitivity at 24 hr, it was predicted that, in the absence of auditory experience, devocal-isolated ducklings would fail to show sufficient endogenously mediated improvement to bring them up to the level of perceptual competence of vocal-communal ducklings at any age. This hypothesis proved wrong in that the proportion of devocalized ducklings showing a preference for the normal maternal call over the greater than 825-Hz attenuated one became equivalent to the vocal ducklings at 48 hr after hatching, as did their ability to discriminate the normal maternal call from greater than 1,800-Hz attenuated maternal call. At 65 hr, however, the devocalized ducklings' performance deteriorated back to the level observed at 24 hr. Embryonic exposure to the (sibling) contact-contentment call prevents the perceptual deficit at 24 hr and the deterioration at 65 hr.     

Long-term memory formation in the chick requires mobilization of ryanodine-sensitive intracellular calcium stores

Training chicks (Gallus domesticus) on a one-trial passive avoidance task results in transient and time-dependent enhanced increases in N-methyl-d-aspartate- or alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate-stimulated intracellular calcium concentration in synaptoneurosomes isolated from a specific forebrain region, the intermediate medial hyperstriatum ventrale. This increase could result from either calcium entry from the extracellular medium or from mobilization of intracellular calcium stores. We have therefore examined the effects of dantrolene, an inhibitor of calcium release from the intracellular ryanodine-sensitive store, on these processes. Dantrolene, 50 nmol per hemisphere injected intracerebrally 30 min pre- or 30 min posttraining, blocked longer term memory for the passive avoidance task, whereas memory for the task was unaffected when dantrolene was injected at earlier or later times. Preincubation of synaptoneurosomes, isolated from the intermediate hyperstriatum ventrale 10 min after training, with 100 nM dantrolene abolished the enhanced training-induced increase in intracellular calcium concentration elicited by 0.5 mM N-methyl-d-aspartate. By contrast, the training-induced enhancement of the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate-stimulated increase in intracellular calcium concentration in synaptoneurosomes prepared 6 h posttraining was unaffected by preincubation with dantrolene, which was not amnestic at this time. Calcium release from ryanodine-sensitive intracellular stores may thus be a necessary stage in the early phase of the molecular cascade leading to the synaptic modulation required for long-term memory storage.     

Experience with songs in adulthood reduces song-induced gene expression in songbird auditory forebrain

Male songbirds learn to produce song within a limited phase early in life; however they continue to learn to recognize songs in adulthood. Studies looking at Zenk activation after exposure to songs learned early in life for song production and songs learned in adulthood show opposite patterns of activation, suggesting distinct neural mechanisms may be involved in these two forms of learning. In this study, we look at IEG Zenk activation in auditory regions NCM and CMM of song sparrows (Melospiza melodia) to see whether recent exposure to song in adulthood leads to greater or decreased Zenk activation upon hearing that song versus a novel song. We found significantly lower activation in birds exposed to previously heard songs versus novel songs in vNCM but not dNCM, though further analysis suggest an overall trend in NCM. We found no significant difference in the amount of activation to previously heard songs vs. novel songs in CMM. These results support previous findings suggesting that activation is reduced to learned stimuli; we discuss possible implications of these findings in relation to song production learning early in life and song recognition learning in adulthood.     

The influences of listening and speaking on pedestrians' assessments of approaching vehicles

Research suggests a relationship between auditory distraction (such as environmental noises or a vocal cell phone conversation) and a decreased ability to detect and localize approaching vehicles. What is unclear is whether auditory vehicle perception is impacted more by distractions reliant on listening or distractions reliant on speaking (analogous to the two components of a vocal cell phone conversation). In two experiments, adult participants listened for approaching vehicle noises and while performing listening- and speaking-based secondary tasks. Participants were tasked with identifying when they first detect an approaching vehicle and when they no longer felt safe to cross in front of the approaching vehicle. For both experiments, the speaking task resulted in significantly later detection of approaching vehicles and riskier crossing thresholds than in the no-distraction and listening conditions. The listening secondary task significantly differed from the control condition in experiment 1, but not experiment 2. Overall, our results suggest auditory distractions, particularly those reliant on speaking, negatively impact pedestrian safety in situations where visual information is minimal. Results may provide guidance for future research and policy about the safety impacts of secondary tasks.     

Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus)

Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species' vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.     

A Markov Chain Analysis of Emotional Exchange in Voice‐to‐Voice Communication: Testing for the Mimicry Hypothesis of Emotional Contagion

Mimicry is a central plank of the emotional contagion theory; however, it was only tested with facial and postural emotional stimuli. This study explores the existence of mimicry in voice‐to‐voice communication by analyzing 8,747 sequences of emotional displays between customers and employees in a call‐center context. We listened live to 967 telephone interactions, registered the sequences of emotional displays, and analyzed them with a Markov chain. We also explored other propositions of emotional contagion theory that were yet to be tested in vocal contexts. Results supported that mimicry is significantly present at all levels. Our findings fill an important gap in the emotional contagion theory; have practical implications regarding voice‐to‐voice interactions; and open doors for future vocal mimicry research.     

听觉中脑声定位的机制

人和动物对声源方位的感知和心理确定建立在神经生理基础之上,得到了大量来自神经细胞电生理研究证据的支持。听中枢神经元可通过比较到达两耳声信号的不同特征和参量来体现其精确的声源定位能力。研究表明,声源定位过程是听觉系统复杂综合作用的结果,听觉中脑核团-下丘在这一过程中起着重要作用,下丘中大量双耳听觉反应神经元可编码声音(源)方位信息,甚至双侧下丘间的联合投射也有可能参与双耳听觉反应的调制。     

Stimulus generalization of conditioned eyelid responses produced without cerebellar cortex: implications for plasticity in the cerebellar nuclei

In Pavlovian eyelid conditioning and adaptation of the vestibulo-ocular reflex, cerebellar cortex lesions fail to completely abolish previously acquired learning, indicating an additional site of plasticity in the deep cerebellar or vestibular nucleus. Three forms of plasticity are known to occur in the deep cerebellar nuclei: formation of new synapses, plasticity at existing synapses, and changes in intrinsic excitability. Only a cell-wide increase in excitability predicts that learning should generalize broadly from a training stimulus to other stimuli capable of supporting learning, whereas the alternatives predict that learning should be relatively specific to the training stimulus. Here we show that deep nucleus plasticity, as assessed by conditioned eyelid responses produced without input from the cerebellar cortex, is relatively specific to the training conditioned stimulus (CS). We trained rabbits to a tone or light CS with periorbital stimulation as the unconditioned stimulus (US), and pharmacologically disconnected the cerebellar cortex during a posttraining generalization test. The short-latency conditioned responses unmasked by this treatment showed strong decrement along the dimension of auditory frequency and did not generalize across stimulus modalities. These results cannot be explained solely by a cell-wide increase in the excitability of deep nucleus neurons, and imply that an input-specific mechanism in the deep cerebellar nucleus operates as well.     

Development of species identification in ducklings: I. Nature of perceptual deficit caused by embryonic auditory deprivation.

In simultaneous choice tests with normal and filtered maternal calls, devocal-isolated ducklings were much more likely than vocal-communal ducklings to select the mallard maternal call in which the higher frequencies were severely attenuated, thus indicating their relative insensitivity to the higher frequency components of the maternal call. On the other hand, the devocal ducklings were as adept as vocal ducklings in selecting the normal mallard maternal cal1 when it was pitted against a low-frequency attenuated mallard call. Thus, the perceptual deficiency resulting from embryonic and postnatal auditory deprivation is selective in the sense of being relegated to the higher frequency components of the maternal call. Devocalization prevents the embryo and hatchling from hearing their own vocalizations all of which happen to be in the high-frequency range (greater than or equal to 1,500 Hz).