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Olfactory learning and memory in the greater short-nosed fruit bat Cynopterus sphinx: the influence of conspecifics distress calls

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Koilmani Emmanuvel Rajan at Bharathidasan University
Koilmani Emmanuvel Rajan
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Abstract and Figures

This study was designed to test whether Cynopterus sphinx distress calls influence olfactory learning and memory in conspecifics. Bats were exposed to distress calls/playbacks (PBs) of distress calls/modified calls and were then trained to novel odors. Bats exposed to distress calls/PBs made significantly fewer feeding attempts and bouts of PBs exposed to modified calls, which significantly induced the expression of c-Fos in the caudomedial neostriatum (NCM) and the amygdala compared to bats exposed to modified calls and trained controls. However, the expression of c-Fos in the hippocampus was not significantly different between the experimental groups. Further, protein phosphatase-1 (PP-1) expression was significantly lower, and the expression levels of E1A homologue of CREB-binding protein (CBP) (P300), brain-derived neurotrophic factor (BDNF) and its tyrosine kinase B1 (TrkB1) receptor were significantly higher in the hippocampus of control/bats exposed to modified calls compared to distress calls/PBs of distress call-exposed bats. Exposure to the call possibly alters the reciprocal interaction between the amygdala and the hippocampus, accordingly regulating the expression levels of PP1, P300 and BDNF and its receptor TrkB1 following training to the novel odor. Thus, the learning and memory consolidation processes were disrupted and showed fewer feeding attempts and bouts. This model may be helpful for understanding the contributions of stressful social communications to human disorders.
Free-ranging C. sphinx distress call after becoming trapped in a mist net. a Oscillogram of a continuous distress call, with narrowband arched frequency modulation (nAFM) and broadband arched frequency modulation (bAFM) fused together and alternating continuously. b Spectrogram of continuous distress calls indicating harmonics. c Relative power spectrum depicting peak frequencies of the distress call
Free-ranging C. sphinx distress call after becoming trapped in a mist net. a Oscillogram of a continuous distress call, with narrowband arched frequency modulation (nAFM) and broadband arched frequency modulation (bAFM) fused together and alternating continuously. b Spectrogram of continuous distress calls indicating harmonics. c Relative power spectrum depicting peak frequencies of the distress call
… 
The modified distress call of C. sphinx shows variation in a the oscillogram, with nAFM and nAFM fused together and then bAFM and bAFM alternating continuously. b Spectrogram of modified calls indicating altered harmonics. c Relative power spectrum depicting peak frequencies of the modified distress call
The modified distress call of C. sphinx shows variation in a the oscillogram, with nAFM and nAFM fused together and then bAFM and bAFM alternating continuously. b Spectrogram of modified calls indicating altered harmonics. c Relative power spectrum depicting peak frequencies of the modified distress call
… 
The specific structure of distress calls influences the olfactory learning and memory of C. sphinx conspecifics. Behavioural responses of C. sphinx to the novel odour during a training and b retention tests. Data are shown as the mean ± SEM, *indicates a significant difference (***P 0.001) with respect to comparisons within groups (a Con vs Distress call; b Con vs PB distress call; c modified call vs PB distress call; d modified call vs distress call)
The specific structure of distress calls influences the olfactory learning and memory of C. sphinx conspecifics. Behavioural responses of C. sphinx to the novel odour during a training and b retention tests. Data are shown as the mean ± SEM, *indicates a significant difference (***P 0.001) with respect to comparisons within groups (a Con vs Distress call; b Con vs PB distress call; c modified call vs PB distress call; d modified call vs distress call)
… 
The specific structure of the distress call promotes c-Fos expression in the caudomedial neostriatum (NCM) of C. sphinx. Bats were allowed to listen to the distress call/PB of the distress call/modified call and were trained to a novel odour after 15 min. a Representative western blots showing the expression patterns of c-Fos in the NCM regions of experimental groups. Estimated levels of b c-Fos expression showing significant differences (*P < 0.05; ***P < 0.001) between groups (a Con vs Distress call; b Con vs PB distress call; c distress call vs modified call; d PB distress calls vs modified call; e Con vs Modified call)
The specific structure of the distress call promotes c-Fos expression in the caudomedial neostriatum (NCM) of C. sphinx. Bats were allowed to listen to the distress call/PB of the distress call/modified call and were trained to a novel odour after 15 min. a Representative western blots showing the expression patterns of c-Fos in the NCM regions of experimental groups. Estimated levels of b c-Fos expression showing significant differences (*P < 0.05; ***P < 0.001) between groups (a Con vs Distress call; b Con vs PB distress call; c distress call vs modified call; d PB distress calls vs modified call; e Con vs Modified call)
… 
Conspecific distress calls with specific structures induce the expression of c-Fos in the amygdala of C. sphinx. Bats were allowed to listen to the distress call/PB of the distress call/modified call and were trained to a novel odour after 15 min. a Representative western blots showing the expression patterns of c-Fos in the amygdala in the experimental groups. Estimated levels of b c-Fos expression showing significant differences (*P < 0.05; ***P < 0.001) between groups (a Con vs distress call; b Con vs PB distress call; c distress call vs modified call; d PB distress calls vs modified call; e Con vs modified call)
+4
Conspecific distress calls with specific structures induce the expression of c-Fos in the amygdala of C. sphinx. Bats were allowed to listen to the distress call/PB of the distress call/modified call and were trained to a novel odour after 15 min. a Representative western blots showing the expression patterns of c-Fos in the amygdala in the experimental groups. Estimated levels of b c-Fos expression showing significant differences (*P < 0.05; ***P < 0.001) between groups (a Con vs distress call; b Con vs PB distress call; c distress call vs modified call; d PB distress calls vs modified call; e Con vs modified call)
… 
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Vol.:(0123456789)
1 3
Journal of Comparative Physiology A (2021) 207:667–679
https://doi.org/10.1007/s00359-021-01505-2
ORIGINAL PAPER
Olfactory learning andmemory inthegreater short‑nosed fruit bat
Cynopterus sphinx: theinfluence ofconspecifics distress calls
KoilmaniEmmanuvelRajan1
Received: 20 September 2020 / Revised: 13 July 2021 / Accepted: 4 August 2021 / Published online: 23 August 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract
This study was designed to test whether Cynopterus sphinx distress calls influence olfactory learning and memory in con-
specifics. Bats were exposed to distress calls/playbacks (PBs) of distress calls/modified calls and were then trained to novel
odors. Bats exposed to distress calls/PBs made significantly fewer feeding attempts and bouts of PBs exposed to modified
calls, which significantly induced the expression of c-Fos in the caudomedial neostriatum (NCM) and the amygdala com-
pared to bats exposed to modified calls and trained controls. However, the expression of c-Fos in the hippocampus was not
significantly different between the experimental groups. Further, protein phosphatase-1 (PP-1) expression was significantly
lower, and the expression levels of E1A homologue of CREB-binding protein (CBP) (P300), brain-derived neurotrophic
factor (BDNF) and its tyrosine kinase B1 (TrkB1) receptor were significantly higher in the hippocampus of control/bats
exposed to modified calls compared to distress calls/PBs of distress call-exposed bats. Exposure to the call possibly alters
the reciprocal interaction between the amygdala and the hippocampus, accordingly regulating the expression levels of PP1,
P300 and BDNF and its receptor TrkB1 following training to the novel odor. Thus, the learning and memory consolidation
processes were disrupted and showed fewer feeding attempts and bouts. This model may be helpful for understanding the
contributions of stressful social communications to human disorders.
Keywords Olfactory learning· Cynopterus sphinx· Distress calls· c-Fos· Brain-derived neurotrophic factor (BDNF)
Abbreviations
ALP Alkaline phosphatase
bAFM Broadband arched frequency modulation
BCIP 5-Bromo-4-chloro-3-indolylphosphate
disodium
BDNF Brain-derived neurotrophic factor
CREB-1 Cyclic AMP response element binding
protein-1
ERK-1/2 Extracellular-signal-regulated kinase-1/2
GAPDH Glyceraldehydes-3-phosphate dehydrogenase
IEG Immediate early gene
LTP Long-term potentiation
nAFM Narrow band arched frequency modulation
NBT Nitro-blue tetrazoliumchloride
NCM Caudomedial neostriatum
PBs Playbacks
PKA Protein kinase A
PP-1 Protein phosphatase-1
TrkB1 Tyrosine kinase B1
Introduction
Acoustic communication plays a significant role in informa-
tion exchange between conspecifics (Fenton 2003; Gladziola
etal. 2012; Hörmann etal. 2020). Conspecific communica-
tions are discrete acoustic structures that readily discrimi-
nate and transmit the intentional state of emitters to potential
receivers, termed “social calls”. Earlier studies reported that
social calls’ acoustic structures are context-specific, such
as mother–pup reunion (Knörnschild etal. 2013), forag-
ing coordination (Wright etal. 2014), group recognition
(Budenz etal. 2009), mate attraction (Knörnschild etal.
2014) and distress (Huang etal. 2015). Distress calls are
produced during stressful situations such as extreme physi-
cal stress (Russ etal. 2005; Carter etal. 2015; Walter and
Schnitzler 2019) or when being threatened/attacked by a
predator (Lima and Ó Keefe 2013; Huang etal. 2015). The
* Koilmani Emmanuvel Rajan
emmanuvel1972@yahoo.com
1 Behavioural Neuroscience Laboratory, Department
ofAnimal Science, School ofLife Sciences, Bharathidasan
University, Tiruchirappalli620024, India
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
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  • May 2021
  • CELL MOL NEUROBIOL
Exposure to noise produces cognitive and emotional disorders, and recent studies have shown that auditory stimulation or deprivation affects hippocampal function. Previously, we showed that exposure to high-intensity sound (110 dB, 1 min) strongly inhibits Schaffer-CA1 long-term potentiation (LTP). Here we investigated possible mechanisms involved in this effect. We found that exposure to 110 dB sound activates c-fos expression in hippocampal CA1 and CA3 neurons. Although sound stimulation did not affect glutamatergic or GABAergic neurotransmission in CA1, it did depress the level of brain-derived neurotrophic factor (BDNF), which is involved in promoting hippocampal synaptic plasticity. Moreover, perfusion of slices with BDNF rescued LTP in animals exposed to sound stimulation, whereas BDNF did not affect LTP in sham-stimulated rats. Furthermore, LM22A4, a TrkB receptor agonist, also rescued LTP from sound-stimulated animals. Our results indicate that depression of hippocampal BDNF mediates the inhibition of LTP produced by high-intensity sound stimulation.
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Bats distress vocalizations carry fast amplitude modulations that could represent an acoustic correlate of roughness
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Full-text available
  • Apr 2020
Communication sounds are ubiquitous in the animal kingdom, where they play a role in advertising physiological states and/or socio-contextual scenarios. Human screams, for example, are typically uttered in fearful contexts and they have a distinctive feature termed as “roughness”, which depicts amplitude fluctuations at rates from 30–150 Hz. In this article, we report that the occurrence of fast acoustic periodicities in harsh sounding vocalizations is not unique to humans. A roughness-like structure is also present in vocalizations emitted by bats (species Carollia perspicillata) in distressful contexts. We report that 47.7% of distress calls produced by bats carry amplitude fluctuations at rates ~1.7 kHz (>10 times faster than temporal modulations found in human screams). In bats, rough-like vocalizations entrain brain potentials and are more effective in accelerating the bats’ heart rate than slow amplitude modulated sounds. Our results are consistent with a putative role of fast amplitude modulations (roughness in humans) for grabbing the listeners attention in situations in which the emitter is in distressful, potentially dangerous, contexts.
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Activation in human auditory cortex in relation to the loudness and unpleasantness of low-frequency and infrasound stimuli
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Full-text available
Low frequency noise (LFS) and infrasound (IS) are controversially discussed as potential causes of annoyance and distress experienced by many people. However, the perception mechanisms for IS in the human auditory system are not completely understood yet. In the present study, sinusoids at 32 Hz (at the lower limit of melodic pitch for tonal stimulation), as well as 8 Hz (IS range) were presented to a group of 20 normal hearing subjects, using monaural stimulation via a loudspeaker sound source coupled to the ear canal by a long silicone rubber tube. Each participant attended two experimental sessions. In the first session, participants performed a categorical loudness scaling procedure as well as an unpleasantness rating task in a sound booth. In the second session, the loudness scaling procedure was repeated while brain activation was measured using functional magnetic resonance imaging (fMRI). Subsequently, activation data were collected for the respective stimuli presented at fixed levels adjusted to the individual loudness judgments. Silent trials were included as a baseline condition. Our results indicate that the brain regions involved in processing LFS and IS are similar to those for sounds in the typical audio frequency range, i.e., mainly primary and secondary auditory cortex (AC). In spite of large variation across listeners with respect to judgments of loudness and unpleasantness, neural correlates of these interindividual differences could not yet be identified. Still, for individual listeners, fMRI activation in the AC was more closely related to individual perception than to the physical stimulus level.
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Distress calls of nectarivorous bats (Glossophaga soricina) encode individual and species identity
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Full-text available
  • Feb 2020
Distress calls are known from a variety of animals and are defined as vocalisations emitted during extreme physical stress. Even though distress calls have been studied for a long time, their precise advantage for callers or the significance for receivers is still unclear. In this study, we describe distress calls of the nectarivorous bat Glossophaga soricina (Phyllostomidae: Glossophaginae). Analysing 1925 distress call syllables from 15 individuals caught in the field, we defined six different syllable types. Distress calls were high-intensity, broadband sounds with a low frequency range and thus comparable to those of other taxa. We found statistical evidence for an individual signature in distress calls, but not for a sex-specific signature. Further, playback experiments revealed that group-housed bats responded to distress calls, whereas single-housed bats did not, suggesting that the bats' response behaviour is influenced by group size. Bats responded significantly to normal and distorted conspecific distress calls but not to heterospecific distress calls. We found no sex-specific differences in the response to different playback stimuli. In conclusion, our results indicate that distress calls of bats encode important social information that can be used by receivers and that the response behaviour of receivers depends on the presence of conspecifics.
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Branched-chain amino acids mediate resilience to chronic social defeat stress by activating BDNF/TRKB signaling
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Full-text available
  • May 2019
How individuals respond to chronic stress varies. Susceptible individuals ultimately develop depression; whereas resilient individuals live normally. In this study, our objective was to examine the effect of branched-chain amino acids (BCAA), commonly used by athletes, on susceptibility to stress. Male C57BL/6 mice were subjected to daily defeat sessions by a CD1 aggressor, for 10 days. On day11, the behavior of mice was assessed using the social interaction test, elevated plus maze and open field. Mice received the BCAA leucine, isoleucine or valine before each defeat session. Furthermore, we examined whether BCAA regulate brain derived neurotrophic factor (BDNF) signaling by using a brain-permeable tropomyosin receptor kinase B (TRKB) inhibitor, ANA-12. We also tested the effect of voluntary exercise and high protein diets on susceptibility to stress. Mice exposed to chronic stress displayed increased susceptibility and social avoidance. BCAA promoted resilience to chronic stress, rescued social avoidance behaviors and increased hippocampal BDNF levels and TRKB activation. Inhibition of TRKB signaling abolished the ability of BCAA to promote resilience to stress and to rescue social avoidance. Interestingly, we found that BCAA activate the exercise-regulated PGC1a/FNDC5 pathway known to induce hippocampal BDNF signaling. Although both voluntary exercise and BCAA promoted resilience to stress, combining them did not yield synergistic effects confirming that they affect similar pathways. We also discovered that high protein diets mimic the effect of BCAA by rescuing social deficits induced by chronic stress and increase Bdnf expression in the hippocampus. Our data indicate that BCAA, exercise and high protein diets rescue susceptibility to stress by activating the hippocampal BDNF/TRKB signaling.
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Intra‐Amygdala Metaplasticity Modulation of Fear Extinction Learning.
Article
  • Dec 2020
The amygdala is a key brain region involved in emotional memory formation. It is also responsible for memory modulation in other brain areas. Under extreme conditions, amygdala modulation may lead to the generation of abnormal plasticity and trauma‐related psychopathologies. However, the amygdala itself is a dynamic brain region, which is amenable to long‐term plasticity and is affected by emotional experiences. These alterations may modify the way the amygdala modulates activity and plasticity in other related brain regions, which in turn may alter the animal’s response to subsequent challenges in what could be termed as ‘Behavioral metaplasticity’. Because of the reciprocal interactions between the amygdala and other emotion processing regions, such as the medial prefrontal cortex (mPFC) or the hippocampus, experience‐induced intra‐amygdala metaplasticity could lead to alterations in mPFC‐dependent or hippocampus‐dependent behaviors. While initiated by alterations within the basolateral amygdala (BLA), such alterations in other brain regions may come to be independent of BLA modulation, thus establishing what may be termed ‘Trans‐regional metaplasticity’. In this article, we review evidence supporting the notions of intra‐BLA metaplasticity and how this may develop into ‘Trans‐regional metaplasticity’. Future research is needed to understand how such dynamic metaplastic alterations contribute to developing psychopathologies, and how this knowledge may be translated into promoting novel interventions in psychopathologies associated with fear, stress, and trauma.
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Processing of fast amplitude modulations in bat auditory cortex matches communication call-specific sound features
Article
  • Feb 2019
Bats use a large repertoire of calls for social communication. In the bat Phyllostomus discolor, social communication calls are often characterized by sinusoidal amplitude and frequency modulations with modulation frequencies in the range of 100-130 Hz. However, peaks in mammalian auditory cortical modulation transfer functions are typically limited to modulation frequencies below 100 Hz. We investigated the coding of sinusoidally amplitude modulated sounds in auditory cortical neurons in P. discolor by constructing rate and temporal modulation transfer functions. Neuronal responses to playbacks of various communication calls were additionally recorded and compared with the neurons' responses to sinusoidally amplitude-modulated sounds. Cortical neurons in the posterior dorsal field of the auditory cortex were tuned to unusually high modulation frequencies: rate modulation transfer functions often peaked around 130 Hz (median: 87 Hz), and the median of the highest modulation frequency that evoked significant phase-locking was also 130 Hz. Both values are much higher than reported from the auditory cortex of other mammals, with more than 51% of the units preferring modulation frequencies exceeding 100 Hz. Conspicuously, the fast modulations preferred by the neurons match the fast amplitude and frequency modulations of prosocial, and mostly of aggressive, communication calls in P. discolor. We suggest that the preference for fast amplitude modulations in the P. discolor dorsal auditory cortex serves to reliably encode the fast modulations seen in their communication calls. NEW & NOTEWORTHY Neural processing of temporal sound features is crucial for the analysis of communication calls. In bats, these calls are often characterized by fast temporal envelope modulations. Because auditory cortex neurons typically encode only low modulation frequencies, it is unclear how species-specific vocalizations are cortically processed. We show that auditory cortex neurons in the bat Phyllostomus discolor encode fast temporal envelope modulations. This property improves response specificity to communication calls and thus might support species-specific communication.
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Localization of Contextual and Context Removed Auditory Fear Memory within the Basolateral Amygdala Complex
Article
  • Feb 2019
  • NEUROSCIENCE
Debilitating and persistent fear memories can rapidly form in humans following exposure to traumatic events. Fear memories can also be generated and studied in animals via Pavlovian fear conditioning. The current study was designed to evaluate basolateral amygdala complex (BLC) involvement following the formation of different fear memories (two contextual fear memories and one adjusted auditory fear memory). Fear memories were created in the same context with five 1.0 mA (0.50 s) foot-shocks and, where necessary, five auditory tones (5 kHz, 75 dB, 20 s). The adjusted auditory fear conditioning protocol was employed to remove background contextual fear and produce isolated auditory fear memories. Immunofluorescent labeling was utilized to identify neurons expressing immediate early genes (IEGs). We found the two contextual fear conditioning (CFC) procedures to produce similar levels of fear-related freezing to context. Contextual fear memories produced increases in BLC IEG expression with distinct and separate patterns of expression. These data suggest contextual fear memories created in slightly altered contexts, can produce unique patterns of amygdala activation. The adjusted auditory fear conditioning procedure produced memories to a tone, but not to a context. This group, where no contextual fear was present, had a significant reduction in BLC IEG expression. These data suggest background contextual fear memories, created in standard auditory fear conditioning protocols, contribute significantly to increases in amygdala activation.
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Odour discrimination learning in the Indian greater short-nosed fruit bat (Cynopterus sphinx): Differential expression of Egr-1, C-fos and PP-1 in the olfactory bulb, amygdala and hippocampus
Article
  • Apr 2018
Activity-dependent expression of immediate-early genes (IEGs) is induced by exposure to odor. The present study was designed to investigate whether there is differential expression of IEGs (Egr-1, C-fos) in the brain region mediating olfactory memory in the Indian greater short-nosed fruit bat Cynopterus sphinx We assumed that differential expression of IEGs in different brain regions may orchestrate a preference odor (PO) and aversive odor (AO) memory in C. sphinx We used preferred (0.8% wt/wt of cinnamon powder) and aversive (0.4% wt/vol of citral) odor substances, with freshly-prepared chopped apple, to assess the behavioural response and induction of IEGs in the olfactory bulb, hippocampus and amygdala. After experiencing PO and AO, the bats initially responded to both, later only engaging in feeding bouts in response to the PO food. The expression pattern of Egr-1 and C-fos in the olfactory bulb, hippocampus and amygdala was similar at different time points (15, 30 and 60 min) following the response to PO, but different for AO. The response to AO elevated the level of C-fos expression within 30 min and reduced it at 60 min in both the olfactory bulb and the hippocampus, as opposed to the continuous increase noted in the amygdala. In addition, we tested whether an epigenetic mechanism entailing protein phosphatase-1 (PP-1) acts on IEG expression. The observed PP-1 expression and the level of unmethylated/methylated promoter revealed that the C-fos expression is possibly controlled by an odor-mediated regulation of PP-1. These results in turn imply that the differential expression of C-fos in the hippocampus and amygdala may contribute to olfactory learning and memory in C. sphinx.
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