Contextual Modulation of Vocal Behavior in Mouse: Newly Identified 12 kHz "Mid-Frequency" Vocalization Emitted during Restraint.
mouse; context; isolation; restraint; stress; vocalization
While several studies have investigated mouse ultrasonic vocalizations (USVs) emitted by isolated pups or by males in mating contexts, studies of behavioral contexts other than mating and vocalization categories other than USVs have been limited. By improving our understanding of the vocalizations emitted by mice across behavioral contexts, we will better understand the natural vocal behavior of mice and better interpret vocalizations from mouse models of disease. Hypothesizing that mouse vocal behavior would differ depending on behavioral context, we recorded vocalizations from male CBA/CaJ mice across three behavioral contexts including mating, isolation, and restraint. We found that brief restraint elevated blood corticosterone levels of mice, indicating increased stress relative to isolation. Further, after 3 days of brief restraint, mice displayed behavioral changes indicative of stress. These persisted for at least 2 days after restraint. Contextual differences in mouse vocal behavior were striking and robust across animals. Thus, while USVs were the most common vocalization type across contexts, the spectrotemporal features of USVs were context-dependent. Compared to the mating context, vocalizations during isolation and restraint displayed a broader frequency range, with a greater emphasis on frequencies below 50 kHz. These contexts also included more non-USV vocal categories and different vocal patterns. We identified a new Mid-Frequency Vocalization, a tonal vocalization with fundamental frequencies below 18 kHz, which was almost exclusively emitted by mice undergoing restraint stress. These differences combine to form vocal behavior that is grossly different among behavioral contexts and may reflect the level of anxiety in these contexts.
Grimsley Jasmine M S; Sheth Saloni; Vallabh Neil; Grimsley Calum A; Bhattal Jyoti; Latsko Maeson; Jasnow Aaron; Wenstrup Jeffrey J
Frontiers in behavioral neuroscience
2016
1905-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fnbeh.2016.00038" target="_blank" rel="noreferrer noopener">10.3389/fnbeh.2016.00038</a>
Automated classification of mouse pup isolation syllables: from cluster analysis to an Excel-based "mouse pup syllable classification calculator".
vocalization; cluster analysis; communication call; isolation calls; mouse pup calls; mouse song
Mouse pups vocalize at high rates when they are cold or isolated from the nest. The proportions of each syllable type produced carry information about disease state and are being used as behavioral markers for the internal state of animals. Manual classifications of these vocalizations identified 10 syllable types based on their spectro-temporal features. However, manual classification of mouse syllables is time consuming and vulnerable to experimenter bias. This study uses an automated cluster analysis to identify acoustically distinct syllable types produced by CBA/CaJ mouse pups, and then compares the results to prior manual classification methods. The cluster analysis identified two syllable types, based on their frequency bands, that have continuous frequency-time structure, and two syllable types featuring abrupt frequency transitions. Although cluster analysis computed fewer syllable types than manual classification, the clusters represented well the probability distributions of the acoustic features within syllables. These probability distributions indicate that some of the manually classified syllable types are not statistically distinct. The characteristics of the four classified clusters were used to generate a Microsoft Excel-based mouse syllable classifier that rapidly categorizes syllables, with over a 90% match, into the syllable types determined by cluster analysis.
Grimsley Jasmine M S; Gadziola Marie A; Wenstrup Jeffrey J
Frontiers in behavioral neuroscience
2012
1905-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fnbeh.2012.00089" target="_blank" rel="noreferrer noopener">10.3389/fnbeh.2012.00089</a>
Glycinergic "inhibition" mediates selective excitatory responses to combinations of sounds.
Animals; Acoustic Stimulation/methods; Neural Inhibition/drug effects/*physiology; *Sound; Excitatory Amino Acid Antagonists/pharmacology; Action Potentials/drug effects/physiology; Auditory Pathways/*physiology; Glycine Agents/pharmacology; Glycine/*physiology; Chiroptera/physiology; Drug Interactions; GABA Agents/pharmacology; Inferior Colliculi/cytology/drug effects/*physiology; Iontophoresis/methods; Neurons/drug effects/physiology/radiation effects; Piperazines/pharmacology; Dose-Response Relationship; Receptors; Radiation; GABA/physiology; N-Methyl-D-Aspartate/antagonists & inhibitors/physiology
In the mustached bat's inferior colliculus (IC), combination-sensitive neurons display time-sensitive facilitatory interactions between inputs tuned to distinct spectral elements in sonar or social vocalizations. Here we compare roles of ionotropic receptors to glutamate (iGluRs), glycine (GlyRs), and GABA (GABA(A)Rs) in facilitatory combination-sensitive interactions. Facilitatory responses to 36 single IC neurons were recorded before, during, and after local application of antagonists to these receptors. The NMDA receptor antagonist CPP [(+/-)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid], alone (n = 14) or combined with AMPA receptor antagonist NBQX (n = 22), significantly reduced or eliminated responses to best frequency (BF) sounds across a broad range of sound levels, but did not eliminate combination-sensitive facilitation. In a subset of neurons, GABA(A)R blockers bicuculline or gabazine were applied in addition to iGluR blockers. GABA(A)R blockers did not "uncover" residual iGluR-mediated excitation, and only rarely eliminated facilitation. In nearly all neurons for which the GlyR antagonist strychnine was applied in addition to iGluR blockade (22 of 23 neurons, with or without GABA(A)R blockade), facilitatory interactions were eliminated. Thus, neither glutamate nor GABA neurotransmission are required for facilitatory combination-sensitive interactions in IC. Instead, facilitation may depend entirely on glycinergic inputs that are presumed to be inhibitory. We propose that glycinergic inputs tuned to two distinct spectral elements in vocal signals each activate postinhibitory rebound excitation. When rebound excitations from two spectral elements coincide, the neuron discharges. Excitation from glutamatergic inputs, tuned to the BF of the neuron, is superimposed onto this facilitatory interaction, presumably mediating responses to a broader range of acoustic signals.
Sanchez Jason Tait; Gans Donald; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2008
2008-01
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/JNEUROSCI.3572-07.2008" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.3572-07.2008</a>
Circuitry underlying spectrotemporal integration in the auditory midbrain.
Female; Male; Time Factors; Animals; Acoustic Stimulation/*methods; Chiroptera; Auditory Pathways/*physiology; Mesencephalon/*physiology; Nerve Net/*physiology
Combination sensitivity in central auditory neurons is a form of spectrotemporal integration in which excitatory responses to sounds at one frequency are facilitated by sounds within a distinctly different frequency band. Combination-sensitive neurons respond selectively to acoustic elements of sonar echoes or social vocalizations. In mustached bats, this response property originates in high-frequency representations of the inferior colliculus (IC) and depends on low and high frequency-tuned glycinergic inputs. To identify the source of these inputs, we combined glycine immunohistochemistry with retrograde tract tracing. Tracers were deposited at high-frequency (\textgreater56 kHz), combination-sensitive recording sites in IC. Most glycine-immunopositive, retrogradely labeled cells were in ipsilateral ventral and intermediate nuclei of the lateral lemniscus (VNLL and INLL), with some double labeling in ipsilateral lateral and medial superior olivary nuclei (LSO and MSO). Generally, double-labeled cells were in expected high-frequency tonotopic areas, but some VNLL and INLL labeling appeared to be in low-frequency representations. To test whether these nuclei provide low frequency-tuned input to the high-frequency IC, we combined retrograde tracing from IC combination-sensitive sites with anterograde tracing from low frequency-tuned sites in the anteroventral cochlear nucleus (AVCN). Only VNLL and INLL contained retrogradely labeled cells near (
Yavuzoglu Asuman; Schofield Brett R; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2011
2011-10
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/JNEUROSCI.3529-11.2011" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.3529-11.2011</a>
Contribution of NMDA and AMPA receptors to temporal patterning of auditory responses in the inferior colliculus.
Animals; Chiroptera/*physiology; Neurons/physiology; Action Potentials/drug effects; Excitatory Amino Acid Antagonists/pharmacology; Quinoxalines/pharmacology; Inferior Colliculi/cytology/drug effects/*physiology; Piperazines/pharmacology; *Acoustic Stimulation; Reaction Time/drug effects/*physiology; N-Methyl-D-Aspartate/*physiology; Receptors; AMPA/*physiology
Although NMDA receptors (NMDARs) are associated with synaptic plasticity, they form an essential part of responses to sensory stimuli. We compared contributions of glutamatergic NMDARs and AMPA receptors (AMPARs) to auditory responses in the inferior colliculus (IC) of awake, adult mustached bats. We examined the magnitude and temporal pattern of responses to tonal signals in single units before, during, and after local micro-iontophoretic application of selective antagonists to AMPARs [NBQX (1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide)] and NMDARs [CPP ((+/-)3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid)]. Combined blockade of AMPARs and NMDARs eliminated excitatory responses in nearly all neurons, whereas separate blockade of each receptor was quantitatively similar, causing substantial (\textgreater 50%) spike reductions in approximately 75% of units. The major result was that effects of receptor blockade were most closely related to the first-spike latency of a unit. Thus, AMPAR blockade substantially reduced spikes in all short-latency units (\textless 12 ms) but never in long-latency units (\textgreater or = 12 ms). NMDAR blockade had variable effects on short-latency units but reduced spikes substantially for all long-latency units. There were no distinct contributions of AMPARs and NMDARs to early and late elements of responses. Thus, AMPAR blockade reduced early (onset) spikes somewhat more effectively than NMDAR blockade in short-latency units, but NMDAR blockade reduced onset spikes more effectively in long-latency units. AMPAR and NMDAR blockade were equally effective in reducing later elements of sustained responses in short-latency units, whereas NMDAR blockade was much more effective in long-latency units. These results indicate that NMDARs play multiple roles for signal processing in adult IC neurons.
Sanchez Jason Tait; Gans Donald; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2007
2007-02
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/JNEUROSCI.2894-06.2007" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.2894-06.2007</a>
Projection to the inferior colliculus from the basal nucleus of the amygdala.
Animals; Acoustic Stimulation/methods; Species Specificity; Action Potentials/physiology; Amygdala/*cytology/physiology; Dextrans; Rhodamines; Fluorescent Dyes; *Stilbamidines; Auditory Cortex/cytology; Auditory Pathways/*cytology/physiology; Axonal Transport/physiology; Brain Stem/cytology; Chiroptera/*anatomy & histology/physiology; Cholera Toxin/pharmacokinetics; Inferior Colliculi/*cytology/physiology; Neurons/cytology/physiology; Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate; Electrodes; Implanted
This report describes a projection from the amygdala, a forebrain center mediating emotional expression, to the inferior colliculus (IC), the midbrain integration center of the ascending auditory system. In the IC of mustached bats (Pteronotus parnellii) and pallid bats (Antrozous pallidus), we placed deposits of retrograde tracers at physiologically defined sites and then searched for retrogradely labeled somata in the forebrain. Labeling was most sensitive in experiments using cholera toxin B-subunit as tracer. We consistently observed retrograde labeling in a single amygdalar subdivision, the magnocellular subdivision of the basal nucleus (Bmg). The Bmg is distinctive across mammals, containing the largest cells in the amygdala and the most intense acetylcholinesterase staining. Labeled amygdalar cells occurred ipsilateral and contralateral to IC deposits, but ipsilateral labeling was greater, averaging 72%. Amygdalar labeling was observed after tracer deposits throughout the IC, including its central nucleus (ICC). In comparison, labeling in the auditory cortex (layer V) was heavily ipsilateral (averaging 92%). Cortical labeling depended on the location of IC deposits: dorsomedial deposits resulted in the most labeled cells, whereas ventrolateral deposits labeled few or no cortical cells. Cortical labeling occurred after several deposits in the ICC. Across experiments, the average number of labeled cells in the amygdala was similar to that in the auditory cortex, indicating that the amygdalocollicular projection is significant. The results demonstrate a direct, widespread projection from the basal amygdala to the IC. They also suggest the presence of a rapid thalamoamygdalocollicular feedback circuit that may impose emotional content onto processing of sensory stimuli at a relatively low level of an ascending sensory pathway.
Marsh Robert A; Fuzessery Zoltan M; Grose Carol D; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2002
2002-12
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/jneurosci.22-23-10449.2002" target="_blank" rel="noreferrer noopener">10.1523/jneurosci.22-23-10449.2002</a>
Coding the meaning of sounds: contextual modulation of auditory responses in the basolateral amygdala.
Female; Male; Animals; Mice; Acoustic Stimulation/*methods; Auditory Perception/*physiology; Action Potentials/*physiology; Amygdala/*physiology; Cats; Animal/*physiology; Inbred CBA; Vocalization
Female mice emit a low-frequency harmonic (LFH) call in association with distinct behavioral contexts: mating and physical threat or pain. Here we report the results of acoustic, behavioral, and neurophysiological studies of the contextual analysis of these calls in CBA/CaJ mice. We first show that the acoustical features of the LFH call do not differ between contexts. We then show that male mice avoid the LFH call in the presence of a predator cue (cat fur) but are more attracted to the same exemplar of the call in the presence of a mating cue (female urine). The males thus use nonauditory cues to determine the meaning of the LFH call, but these cues do not generalize to noncommunication sounds, such as noise bursts. We then characterized neural correlates of contextual meaning of the LFH call in responses of basolateral amygdala (BLA) neurons from awake, freely moving mice. There were two major findings. First, BLA neurons typically displayed early excitation to all tested behaviorally aversive stimuli. Second, the nonauditory context modulates the BLA population response to the LFH call but not to the noncommunication sound. These results suggest that the meaning of communication calls is reflected in the spike discharge patterns of BLA neurons.
Grimsley Jasmine M S; Hazlett Emily G; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2013
2013-10
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/JNEUROSCI.2205-13.2013" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.2205-13.2013</a>
Social vocalizations of big brown bats vary with behavioral context.
Animals; *Animal Communication; Chiroptera/*physiology; Electrocardiography; Acoustics; *Behavior; Animal
Bats are among the most gregarious and vocal mammals, with some species demonstrating a diverse repertoire of syllables under a variety of behavioral contexts. Despite extensive characterization of big brown bat (Eptesicus fuscus) biosonar signals, there have been no detailed studies of adult social vocalizations. We recorded and analyzed social vocalizations and associated behaviors of captive big brown bats under four behavioral contexts: low aggression, medium aggression, high aggression, and appeasement. Even limited to these contexts, big brown bats possess a rich repertoire of social vocalizations, with 18 distinct syllable types automatically classified using a spectrogram cross-correlation procedure. For each behavioral context, we describe vocalizations in terms of syllable acoustics, temporal emission patterns, and typical syllable sequences. Emotion-related acoustic cues are evident within the call structure by context-specific syllable types or variations in the temporal emission pattern. We designed a paradigm that could evoke aggressive vocalizations while monitoring heart rate as an objective measure of internal physiological state. Changes in the magnitude and duration of elevated heart rate scaled to the level of evoked aggression, confirming the behavioral state classifications assessed by vocalizations and behavioral displays. These results reveal a complex acoustic communication system among big brown bats in which acoustic cues and call structure signal the emotional state of a caller.
Gadziola Marie A; Grimsley Jasmine M S; Faure Paul A; Wenstrup Jeffrey J
PloS one
2012
1905-7
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1371/journal.pone.0044550" target="_blank" rel="noreferrer noopener">10.1371/journal.pone.0044550</a>
Development of social vocalizations in mice.
Female; Male; Animals; Mice; *Social Behavior; Acoustics; Aging/physiology; Phonetics; Sound Spectrography; Nonlinear Dynamics; Vocal Cords/physiology; Newborn; Animal/*physiology; Vocalization
Adult mice are highly vocal animals, with both males and females vocalizing in same sex and cross sex social encounters. Mouse pups are also highly vocal, producing isolation vocalizations when they are cold or removed from the nest. This study examined patterns in the development of pup isolation vocalizations, and compared these to adult vocalizations. In three litters of CBA/CaJ mice, we recorded isolation vocalizations at ages postnatal day 5 (p5), p7, p9, p11, and p13. Adult vocalizations were obtained in a variety of social situations. Altogether, 28,384 discrete vocal signals were recorded using high-frequency-sensitive equipment and analyzed for syllable type, spectral and temporal features, and the temporal sequencing within bouts. We found that pups produced all but one of the 11 syllable types recorded from adults. The proportions of syllable types changed developmentally, but even the youngest pups produced complex syllables with frequency-time variations. When all syllable types were pooled together for analysis, changes in the peak frequency or the duration of syllables were small, although significant, from p5 through p13. However, individual syllable types showed different, large patterns of change over development, requiring analysis of each syllable type separately. Most adult syllables were substantially lower in frequency and shorter in duration. As pups aged, the complexity of vocal bouts increased, with a greater tendency to switch between syllable types. Vocal bouts from older animals, p13 and adult, had significantly more sequential structure than those from younger mice. Overall, these results demonstrate substantial changes in social vocalizations with age. Future studies are required to identify whether these changes result from developmental processes affecting the vocal tract or control of vocalization, or from vocal learning. To provide a tool for further research, we developed a MATLAB program that generates bouts of vocalizations that correspond to mice of different ages.
Grimsley Jasmine M S; Monaghan Jessica J M; Wenstrup Jeffrey J
PloS one
2011
2011-03
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1371/journal.pone.0017460" target="_blank" rel="noreferrer noopener">10.1371/journal.pone.0017460</a>
Roles of inhibition in creating complex auditory responses in the inferior colliculus: facilitated combination-sensitive neurons.
Acoustic Stimulation/methods; Action Potentials/*physiology; Animals; Auditory Pathways/physiology; Bicuculline/pharmacology; Cell Count; Drug Interactions; GABA Antagonists/pharmacology; Glycine Agents/pharmacology; Inferior Colliculi/*cytology; Iontophoresis/methods; Models; Neural Inhibition/drug effects/*physiology; Neurological; Neurons/classification/drug effects/*physiology/radiation effects; Otters; Reaction Time/*physiology/radiation effects; Regression Analysis; Strychnine/pharmacology; Time Factors; Wakefulness/physiology
We studied roles of inhibition on temporally sensitive facilitation in combination-sensitive neurons from the mustached bat's inferior colliculus (IC). In these integrative neurons, excitatory responses to best frequency (BF) tones are enhanced by much lower frequency signals presented in a specific temporal relationship. Most facilitated neurons (76%) showed inhibition at delays earlier than or later than the delays causing facilitation. The timing of inhibition at earlier delays was closely related to the best delay of facilitation, but the inhibition had little influence on the duration or strength of the facilitatory interaction. Local iontophoretic application of antagonists to receptors for glycine (strychnine, STRY) and gamma-aminobutyric acid (GABA) (bicuculline, BIC) showed that STRY abolished facilitation in 96% of tested units, but BIC eliminated facilitation in only 28%. This suggests that facilitatory interactions are created in IC and reveals a differential role for these neurotransmitters. The facilitation may be created by coincidence of a postinhibitory rebound excitation activated by the low-frequency signal with the BF-evoked excitation. Unlike facilitation, inhibition at earlier delays was not eliminated by application of antagonists, suggesting an origin in lower brain stem nuclei. However, inhibition at delays later than facilitation, like facilitation itself, appears to originate within IC and to be more dependent on glycinergic than GABAergic mechanisms. Facilitatory and inhibitory interactions displayed by these combination-sensitive neurons encode information within sonar echoes and social vocalizations. The results indicate that these complex response properties arise through a series of neural interactions in the auditory brain stem and midbrain.
Nataraj Kiran; Wenstrup Jeffrey J
Journal of neurophysiology
2005
2005-06
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.01152.2004" target="_blank" rel="noreferrer noopener">10.1152/jn.01152.2004</a>
Roles of inhibition in complex auditory responses in the inferior colliculus: inhibited combination-sensitive neurons.
Acoustic Stimulation; Action Potentials/drug effects/physiology; Afferent/drug effects/*physiology; Animals; Auditory; Auditory Pathways/drug effects/*physiology; Bicuculline/pharmacology; Brain Stem/drug effects/*physiology; Chiroptera; Electrophysiology; Evoked Potentials; GABA-A Receptor Antagonists; GABA-A/physiology; Glycine/antagonists & inhibitors/physiology; Inferior Colliculi/*physiology; Neural Inhibition/drug effects/*physiology; Neurons; Receptors; Strychnine/pharmacology
We studied the functional properties and underlying neural mechanisms associated with inhibitory combination-sensitive neurons in the mustached bat's inferior colliculus (IC). In these neurons, the excitatory response to best frequency tones was suppressed by lower frequency signals (usually in the range of 12-30 kHz) in a time-dependant manner. Of 143 inhibitory units, the majority (71%) were type I, in which low-frequency sounds evoked inhibition only. In the remainder, however, the low-frequency inhibitory signal also evoked excitation. Of these, excitation preceded the inhibition in type E/I units (16%), whereas in type I/E units (13%), excitation followed the inhibition. Type E/I and I/E units were distinct in the tuning and threshold sensitivity of low-frequency responses, whereas type I units overlapped the other types in these features. In 71 neurons, antagonists to receptors for glycine [strychnine (STRY)] or GABA [bicuculline (BIC)] were applied microiontophoretically. These antagonists failed to eliminate combination-sensitive inhibition in 92% (STRY), 93% (BIC), and 87% (BIC + STRY) of the type I units tested. However, inhibition was reduced in many neurons. Results were similar for type E/I and I/E inhibitory neurons. The results indicate that there are distinct populations of combination-sensitive inhibited neurons in the IC and that these populations are at least partly independent of glycine or GABAA receptors in the IC. We propose that these populations originate in different brain stem auditory nuclei, that they may be modified by interactions within the IC, and that they may perform different spectrotemporal analyses of vocal signals.
Nataraj Kiran; Wenstrup Jeffrey J
Journal of neurophysiology
2006
2006-04
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.01148.2005" target="_blank" rel="noreferrer noopener">10.1152/jn.01148.2005</a>
Two distinct representations of social vocalizations in the basolateral amygdala.
*Discrimination (Psychology); *Social Behavior; *Vocalization; acoustic communication; Action Potentials; Amygdala/cytology/*physiology; Animal; Animals; bat; Chiroptera; electrocardiogram; Eptesicus fuscus; Female; Heart Rate; Male; Neurons/classification/*physiology; vocalizations
Acoustic communication signals carry information related to the types of social interactions by means of their "acoustic context," the sequencing and temporal emission pattern of vocalizations. Here we describe responses to natural vocal sequences in adult big brown bats (Eptesicus fuscus). We first assessed how vocal sequences modify the internal affective state of a listener (via heart rate). The heart rate of listening bats was differentially modulated by vocal sequences, showing significantly greater elevation in response to moderately aggressive sequences than appeasement or neutral sequences. Next, we characterized single-neuron responses in the basolateral amygdala (BLA) of awake, restrained bats to isolated syllables and vocal sequences. Two populations of neurons distinguished by background firing rates also differed in acoustic stimulus selectivity. Low-background neurons (\textless1 spike/s) were highly selective, responding on average to one tested stimulus. These may participate in a sparse code of vocal stimuli, in which each neuron responds to one or a few stimuli and the population responds to the range of vocalizations across behavioral contexts. Neurons with higher background rates (\textgreater/=1 spike/s) responded broadly to tested stimuli and better represented the timing of syllables within sequences. We found that spike timing information improved the ability of these neurons to discriminate among vocal sequences and among the behavioral contexts associated with sequences compared with a rate code alone. These findings demonstrate that the BLA contains multiple robust representations of vocal stimuli that can provide the basis for emotional/physiological responses to these stimuli.
Gadziola Marie A; Shanbhag Sharad J; Wenstrup Jeffrey J
Journal of neurophysiology
2016
2016-02
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.00953.2015" target="_blank" rel="noreferrer noopener">10.1152/jn.00953.2015</a>
Auditory responses in the cochlear nucleus of awake mustached bats: precursors to spectral integration in the auditory midbrain.
Acoustic Stimulation/methods; Action Potentials/*physiology; Animals; Auditory; Brain Mapping; Brain Stem/*physiology; Chiroptera/*physiology; Cochlear Nucleus/*physiology; Evoked Potentials; Mesencephalon/physiology; Nerve Net/*physiology; Pitch Perception/*physiology; Wakefulness/physiology
In the cochlear nucleus (CN) of awake mustached bats, single- and two-tone stimuli were used to examine how responses in major CN subdivisions contribute to spectrotemporal integrative features in the inferior colliculus (IC). Across CN subdivisions, the proportional representation of frequencies differed. A striking result was the substantial number of units tuned to frequencies \textless23 kHz. Across frequency bands, temporal response patterns, latency, and spontaneous discharge differed. For example, the 23- to 30-kHz representation, which comprises the fundamental of the sonar call, had an unusually high proportion of units with onset responses (39%) and low spontaneous rates (53%). Units tuned to 58-59 kHz, corresponding to the sharply tuned cochlear resonance, had slightly but significantly longer latencies than other bands. In units tuned to frequencies \textgreater30 kHz, 31% displayed a secondary excitatory peak, usually between 10 and 22 kHz. The secondary peak may originate in cochlear mechanisms for some units, but in others it may result from convergent input onto CN neurons. In 20% of units tested with two-tone stimuli, suppression of best frequency (BF) responses was tuned at least an octave below BF. These properties may underlie similar IC responses. However, other forms of spectral interaction present in IC were absent in CN: we found no facilitatory combination-sensitive interactions and very few combination-sensitive inhibitory interactions of the dominant IC type in which inhibition was tuned to 23-30 kHz. Such interactions arise above CN. Distinct forms of spectral integration thus originate at different levels of the ascending auditory pathway.
Marsh Robert A; Nataraj Kiran; Gans Donald; Portfors Christine V; Wenstrup Jeffrey J
Journal of neurophysiology
2006
2006-01
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.00634.2005" target="_blank" rel="noreferrer noopener">10.1152/jn.00634.2005</a>
A novel coding mechanism for social vocalizations in the lateral amygdala.
*Social Behavior; Acoustic Stimulation; Action Potentials/*physiology; Amygdala/*cytology/physiology; Animal/*physiology; Animals; Auditory Pathways/*physiology; Chiroptera; Dextrans/metabolism; Echolocation/physiology; Female; Male; Neurons/*physiology; Reaction Time/physiology; Rhodamines/metabolism; Time Factors; Vocalization
The amygdala plays a central role in evaluating the significance of acoustic signals and coordinating the appropriate behavioral responses. To understand how amygdalar responses modulate auditory processing and drive emotional expression, we assessed how neurons respond to and encode information that is carried within complex acoustic stimuli. We characterized responses of single neurons in the lateral nucleus of the amygdala to social vocalizations and synthetic acoustic stimuli in awake big brown bats. Neurons typically responded to most of the social vocalizations presented (mean = nine of 11 vocalizations) but differentially modulated both firing rate and response duration. Surprisingly, response duration provided substantially more information about vocalizations than did spike rate. In most neurons, variation in response duration depended, in part, on persistent excitatory discharge that extended beyond stimulus duration. Information in persistent firing duration was significantly greater than in spike rate, and the majority of neurons displayed more information in persistent firing, which was more likely to be observed in response to aggressive vocalizations (64%) than appeasement vocalizations (25%), suggesting that persistent firing may relate to the behavioral context of vocalizations. These findings suggest that the amygdala uses a novel coding strategy for discriminating among vocalizations and underscore the importance of persistent firing in the general functioning of the amygdala.
Gadziola Marie A; Grimsley Jasmine M S; Shanbhag Sharad J; Wenstrup Jeffrey J
Journal of neurophysiology
2012
2012-02
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.00422.2011" target="_blank" rel="noreferrer noopener">10.1152/jn.00422.2011</a>
Tinnitus and underlying brain mechanisms.
*Psychoacoustics; Animals; Auditory Pathways/*physiopathology; Brain – Physiology; Brain/*physiopathology; Female; Forecasting; Humans; Limbic System; Male; Needs Assessment; Risk Factors; Severity of Illness Index; Tinnitus – Physiopathology; Tinnitus – Therapy; Tinnitus/etiology/*physiopathology/therapy
PURPOSE OF REVIEW: Tinnitus is the sensation of hearing a sound when no external auditory stimulus is present. Most individuals experience tinnitus for brief, unobtrusive periods. However, chronic sensation of tinnitus affects approximately 17% (44 million people) of the general US population. Tinnitus, usually a benign symptom, can be constant, loud and annoying to the point that it causes significant emotional distress, poor sleep, less efficient activities of daily living, anxiety, depression and suicidal ideation/attempts. Tinnitus remains a major challenge to physicians because its pathophysiology is poorly understood and there are few management options to offer to patients. The purpose of this article is to describe the current understanding of central neural mechanisms in tinnitus and to summarize recent developments in clinical approaches to tinnitus patients. RECENT FINDINGS: Recently developed animal models of tinnitus provide the possibility to determine neuronal mechanisms of tinnitus generation and to test the effects of various treatments. The latest research using animal models has identified a number of abnormal changes, in both auditory and nonauditory brain regions, that underlie tinnitus. Furthermore this research sheds light on cellular mechanisms that are responsible for development of these abnormal changes. SUMMARY: Tinnitus remains a challenging disorder for patients, physicians, audiologists and scientists studying tinnitus-related brain changes. This article reviews recent findings of brain changes in animal models associated with tinnitus and a brief review of clinical approach to tinnitus patients.
Galazyuk Alexander V; Wenstrup Jeffrey J; Hamid Mohamed A
Current opinion in otolaryngology & head and neck surgery
2012
2012-10
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1097/MOO.0b013e3283577b81" target="_blank" rel="noreferrer noopener">10.1097/MOO.0b013e3283577b81</a>
Excitatory and facilitatory frequency response areas in the inferior colliculus of the mustached bat.
Acoustic Stimulation; Animal; Animals; Auditory; Auditory Perception/*physiology; Brain Stem; Chiroptera/*physiology; Echolocation; Evoked Potentials; Inferior Colliculi/*physiology; Neurons/physiology; Vocalization
In the mustached bat's central nucleus of the inferior colliculus (ICC), many neurons display facilitatory or inhibitory responses when presented with two tones of distinctly different frequencies. Our previous studies have focused on spectral interactions between specific frequency bands contained in the bat's sonar vocalization. In this study, we describe excitatory and facilitatory frequency response areas across all frequencies in the mustached bat's audible range. We show that many neurons in the ICC have more extensive frequency interactions than previously documented. We recorded responses of 96 single units to single tones and combinations of two tones. Best frequencies of the units ranged from 59-15 kHz. Forty-one units had a single, excitatory frequency response area. The rest of the units had more complex frequency tuning that included multiple excitatory frequency response areas and facilitatory frequency response areas. Some of the facilitatory frequency interactions were between one sound with energy in a sonar frequency band and a second sound with energy in a non-sonar frequency band. We also found that neurons could be facilitated by more than one additional frequency band. Our findings of extensive frequency interactions in the ICC of the mustached bat suggest that some neurons may be well suited for the analysis of complex sounds, possibly including social communication sounds.
Portfors Christine V; Wenstrup Jeffrey J
Hearing research
2002
2002-06
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/s0378-5955(02)00376-3" target="_blank" rel="noreferrer noopener">10.1016/s0378-5955(02)00376-3</a>
A three-dimensional digital neurological atlas of the mustached bat (Pteronotus parnellii).
*Atlases as Topic; Animals; Auditory Cortex/anatomy & histology/diagnostic imaging; Brain Stem/anatomy & histology/diagnostic imaging; Brain/*anatomy & histology/diagnostic imaging; Chiroptera/*anatomy & histology; Diffusion Tensor Imaging/methods; Imaging; Magnetic Resonance Imaging/*methods; Male; Skull/anatomy & histology/diagnostic imaging; Three-Dimensional/*methods; Tomography; X-Ray Computed/*methods
Substantial knowledge of auditory processing within mammalian nervous systems emerged from neurophysiological studies of the mustached bat (Pteronotus parnellii). This highly social and vocal species retrieves precise information about the velocity and range of its targets through echolocation. Such high acoustic processing demands were likely the evolutionary pressures driving the over-development at peripheral (cochlea), metencephalic (cochlear nucleus), mesencephalic (inferior colliculus), diencephalic (medial geniculate body of the thalamus), and telencephalic (auditory cortex) auditory processing levels in this species. Auditory researchers stand to benefit from a three dimensional brain atlas of this species, due to its considerable contribution to auditory neuroscience. Our MRI-based atlas was generated from 2 sets of image data of an ex-vivo male mustached bat's brain: a detailed 3D-T2-weighted-RARE scan [(59x63 x 85) mum(3)] and track density images based on super resolution diffusion tensor images [(78) mum(3)] reconstructed from a set of low resolution diffusion weighted images using Super-Resolution-Reconstruction (SRR). By surface-rendering these delineations and extrapolating from cortical landmarks and data from previous studies, we generated overlays that estimate the locations of classic functional subregions within mustached bat auditory cortex. This atlas is freely available from our website and can simplify future electrophysiological, microinjection, and neuroimaging studies in this and related species.
Washington Stuart D; Hamaide Julie; Jeurissen Ben; van Steenkiste Gwendolyn; Huysmans Toon; Sijbers Jan; Deleye Steven; Kanwal Jagmeet S; De Groof Geert; Liang Sayuan; Van Audekerke Johan; Wenstrup Jeffrey J; Van der Linden Annemie; Radtke-Schuller Susanne; Verhoye Marleen
NeuroImage
2018
2018-12
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.neuroimage.2018.08.013" target="_blank" rel="noreferrer noopener">10.1016/j.neuroimage.2018.08.013</a>
Neural processing of target distance by echolocating bats: functional roles of the auditory midbrain.
Animals; Auditory Cortex/physiology; Auditory Pathways/*physiology; Auditory Perception/*physiology; Brain Mapping/psychology; Chiroptera/*physiology; Echolocation/*physiology; Inferior Colliculi/*physiology; Models; Neurological; Neurons/physiology
Using their biological sonar, bats estimate distance to avoid obstacles and capture moving prey. The primary distance cue is the delay between the bat's emitted echolocation pulse and the return of an echo. The mustached bat's auditory midbrain (inferior colliculus, IC) is crucial to the analysis of pulse-echo delay. IC neurons are selective for certain delays between frequency modulated (FM) elements of the pulse and echo. One role of the IC is to create these "delay-tuned", "FM-FM" response properties through a series of spectro-temporal integrative interactions. A second major role of the midbrain is to project target distance information to many parts of the brain. Pathways through auditory thalamus undergo radical reorganization to create highly ordered maps of pulse-echo delay in auditory cortex, likely contributing to perceptual features of target distance analysis. FM-FM neurons in IC also project strongly to pre-motor centers including the pretectum and the pontine nuclei. These pathways may contribute to rapid adjustments in flight, body position, and sonar vocalizations that occur as a bat closes in on a target.
Wenstrup Jeffrey J; Portfors Christine V
Neuroscience and biobehavioral reviews
2011
2011-11
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.neubiorev.2010.12.015" target="_blank" rel="noreferrer noopener">10.1016/j.neubiorev.2010.12.015</a>