scholarly journals Contribution of NMDA and AMPA Receptors to Temporal Patterning of Auditory Responses in the Inferior Colliculus

2007 ◽  
Vol 27 (8) ◽  
pp. 1954-1963 ◽  
Author(s):  
J. T. Sanchez ◽  
D. Gans ◽  
J. J. Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Ampa Receptors ◽  
Temporal Patterning ◽  
Auditory Responses

scholarly journals Abnormal development of auditory responses in the inferior colliculus of a mouse model of Fragile X Syndrome

2020 ◽  
Vol 123 (6) ◽  
pp. 2101-2121 ◽  
Author(s):  
Anna O. Nguyen ◽  
Devin K. Binder ◽  
Iryna M. Ethell ◽  
Khaleel A. Razak
Keyword(s):  
Mouse Model ◽  
Inferior Colliculus ◽  
Fragile X Syndrome ◽  
Fragile X ◽  
Autism Spectrum ◽  
Abnormal Development ◽  
Sensory Sensitivity ◽  
Auditory Responses ◽  
Underlying Mechanisms ◽  
Early Developmental

Autism spectrum disorders (ASD) are commonly associated with sensory sensitivity issues, but the underlying mechanisms are unclear. This study presents novel evidence for neural correlates of auditory hypersensitivity in the developing inferior colliculus (IC) in the Fmr1 knockout (KO) mouse, a mouse model of Fragile X Syndrome (FXS), a leading genetic cause of ASD. Responses begin to show genotype differences between postnatal days 14 and 21, suggesting an early developmental treatment window.

Roles of Inhibition in Creating Complex Auditory Responses in the Inferior Colliculus: Facilitated Combination-Sensitive Neurons

2005 ◽  
Vol 93 (6) ◽  
pp. 3294-3312 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Low Frequency ◽  
Auditory Responses ◽  
Auditory Brain Stem ◽  
Neural Interactions ◽  
Lower Brain Stem ◽  
Excitatory Responses ◽  
Sonar Echoes ◽  
Inhibitory Interactions

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 γ-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.

scholarly journals Temporal Features of Spectral Integration in the Inferior Colliculus: Effects of Stimulus Duration and Rise Time

2009 ◽  
Vol 102 (1) ◽  
pp. 167-180 ◽  
Author(s):  
Donald Gans ◽  
Kianoush Sheykholeslami ◽  
Diana Coomes Peterson ◽  
Jeffrey Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Rise Time ◽  
Low Frequency ◽  
Auditory Pathway ◽  
Spectral Integration ◽  
Auditory Responses ◽  
Temporal Features ◽  
Vocal Signals ◽  
Inhibitory Interactions ◽  
Different Levels

This report examines temporal features of facilitation and suppression that underlie spectrally integrative responses to complex vocal signals. Auditory responses were recorded from 160 neurons in the inferior colliculus (IC) of awake mustached bats. Sixty-two neurons showed combination-sensitive facilitation: responses to best frequency (BF) signals were facilitated by well-timed signals at least an octave lower in frequency, in the range 16–31 kHz. Temporal features and strength of facilitation were generally unaffected by changes in duration of facilitating signals from 4 to 31 ms. Changes in stimulus rise time from 0.5 to 5.0 ms had little effect on facilitatory strength. These results suggest that low frequency facilitating inputs to high BF neurons have phasic-on temporal patterns and are responsive to stimulus rise times over the tested range. We also recorded from 98 neurons showing low-frequency (11–32 kHz) suppression of higher BF responses. Effects of changing duration were related to the frequency of suppressive signals. Signals <23 kHz usually evoked suppression sustained throughout signal duration. This and other features of such suppression are consistent with a cochlear origin that results in masking of responses to higher, near-BF signal frequencies. Signals in the 23- to 30-kHz range—frequencies in the first sonar harmonic—generally evoked phasic suppression of BF responses. This may result from neural inhibitory interactions within and below IC. In many neurons, we observed two or more forms of the spectral interactions described here. Thus IC neurons display temporally and spectrally complex responses to sound that result from multiple spectral interactions at different levels of the ascending auditory pathway.

Analysis of the Role of Inhibition in Shaping Responses to Sinusoidally Amplitude-Modulated Signals in the Inferior Colliculus

1998 ◽  
Vol 80 (4) ◽  
pp. 1686-1701 ◽  
Author(s):  
R. Michael Burger ◽  
George D. Pollak
Keyword(s):  
Nmda Receptors ◽  
Inferior Colliculus ◽  
Ampa Receptors ◽  
Phase Locking ◽  
Receptor Blocker ◽  
Response Property ◽  
Medial Superior Olive ◽  
Competitive Antagonist ◽  
Modulated Signals

Burger, R. Michael and George D. Pollak. Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. J. Neurophysiol. 80: 1686–1701, 1998. Neurons in the central nucleus of the inferior colliculus (ICc) typically respond with phase-locked discharges to low rates of sinusoidal amplitude-modulated (SAM) signals and fail to phase-lock to higher SAM rates. Previous studies have shown that comparable phase-locking to SAM occurs in the dorsal nucleus of the lateral lemniscus (DNLL) and medial superior olive (MSO) of the mustache bat. The studies of MSO and DNLL also showed that the restricted phase-locking to low SAM rates is created by the coincidence of phase-locked excitatory and inhibitory inputs that have slightly different latencies. Here we tested the hypothesis that responses to SAM in the mustache bat IC are shaped by the same mechanism that shapes responses to SAM in the two lower nuclei. We recorded responses from ICc neurons evoked by SAM signals before and during the iontophoretic application of several pharmacological agents: bicuculline, a competitive antagonist for γ-aminobutyric acid-A (GABAA) receptors; strychnine, a competitive antagonist for glycine receptors; the GABAB receptor blocker, phaclofen, and the N-methyl-d-aspartate (NMDA) receptor blocker, (−)-2-amino-5-phosphonopentanoic acid (AP5). The hypothesis that inhibition shapes responses to SAM signals in the ICc was not confirmed. In >90% of the ICc neurons tested, the range of SAM rates to which they phase-locked was unchanged after blocking inhibition with bicuculline, strychnine or phaclofen, applied either individually or in combination. We also considered the possibility that faster α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptors follow high temporal rates of incoming excitation but that the slower NMDA receptors could follow only lower rates. Thus at higher SAM rates, NMDA receptors might generate a sustained excitation that “smears” the phase-locked excitation generated by the AMPA receptors. The NMDA hypothesis, like the inhibition hypothesis, was also not confirmed. In none of the cells that we tested did the application of AP5 by itself, or in combination with bicuculline, cause an increase in the range of SAM rates that evoked phase-locking. These results illustrate that the same response property, phase-locking restricted to low SAM rates, is formed in more than one way in the auditory brain stem. In the MSO and DNLL, the mechanism is coincidence of phase-locked excitation and inhibition, whereas in ICc the same response feature is formed by a different but unknown mechanism.

scholarly journals Visual Modulation of Auditory Responses in the Owl Inferior Colliculus

2009 ◽  
Vol 101 (6) ◽  
pp. 2924-2933 ◽  
Author(s):  
Joseph F. Bergan ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Visual Stimulus ◽  
Visual Stimuli ◽  
Stimulus Presentation ◽  
Neural Responses ◽  
Auditory Space ◽  
Auditory Responses ◽  
Auditory Space Map ◽  
Visual Modulation ◽  
Auditory Plasticity

The barn owl's central auditory system creates a map of auditory space in the external nucleus of the inferior colliculus (ICX). Although the crucial role visual experience plays in the formation and maintenance of this auditory space map is well established, the mechanism by which vision influences ICX responses remains unclear. Surprisingly, previous experiments have found that in the absence of extensive pharmacological manipulation, visual stimuli do not drive neural responses in the ICX. Here we investigated the influence of dynamic visual stimuli on auditory responses in the ICX. We show that a salient visual stimulus, when coincident with an auditory stimulus, can modulate auditory responses in the ICX even though the same visual stimulus may elicit no neural responses when presented alone. For each ICX neuron, the most effective auditory and visual stimuli were located in the same region of space. In addition, the magnitude of the visual modulation of auditory responses was dependent on the context of the stimulus presentation with novel visual stimuli eliciting consistently larger response modulations than frequently presented visual stimuli. Thus the visual modulation of ICX responses is dependent on the characteristics of the visual stimulus as well as on the spatial and temporal correspondence of the auditory and visual stimuli. These results demonstrate moment-to-moment visual enhancements of auditory responsiveness that, in the short-term, increase auditory responses to salient bimodal stimuli and in the long-term could serve to instruct the adaptive auditory plasticity necessary to maintain accurate auditory orienting behavior.

scholarly journals Emergence of Multiplicative Auditory Responses in the Midbrain of the Barn Owl

2007 ◽  
Vol 98 (3) ◽  
pp. 1181-1193 ◽  
Author(s):  
Brian J. Fischer ◽  
José Luis Peña ◽  
Masakazu Konishi
Keyword(s):  
Inferior Colliculus ◽  
Interaural Time Difference ◽  
Extracellular Recording ◽  
Auditory Pathway ◽  
Barn Owl ◽  
Central Nucleus ◽  
Interaural Level Difference ◽  
Tyto Alba ◽  
Neural Responses ◽  
Auditory Responses

Space-specific neurons in the barn owl's auditory space map gain spatial selectivity through tuning to combinations of the interaural time difference (ITD) and interaural level difference (ILD). The combination of ITD and ILD in the subthreshold responses of space-specific neurons in the external nucleus of the inferior colliculus (ICx) is well described by a multiplication of ITD- and ILD-dependent components. It is unknown, however, how ITD and ILD are combined at the site of ITD and ILD convergence in the lateral shell of the central nucleus of the inferior colliculus (ICcl) and therefore whether ICx is the first site in the auditory pathway where multiplicative tuning to ITD- and ILD-dependent signals occurs. We used extracellular recording of single neurons to determine how ITD and ILD are combined in ICcl of the anesthetized barn owl ( Tyto alba). A comparison of additive, multiplicative, and linear-threshold models of neural responses shows that ITD and ILD are combined nonlinearly in ICcl, but the interaction of ITD and ILD is not uniformly multiplicative over the sample. A subset (61%) of the neural responses is well described by the multiplicative model, indicating that ICcl is the first site where multiplicative tuning to ITD- and ILD-dependent signals occurs. ICx, however, is the first site where multiplicative tuning is observed consistently. A network model shows that a linear combination of ICcl responses to ITD–ILD pairs is sufficient to produce the multiplicative subthreshold responses to ITD and ILD seen in ICx.

scholarly journals Roles of Inhibition in Complex Auditory Responses in the Inferior Colliculus: Inhibited Combination-Sensitive Neurons

2006 ◽  
Vol 95 (4) ◽  
pp. 2179-2192 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Low Frequency ◽  
Neural Mechanisms ◽  
The Other ◽  
Inhibitory Neurons ◽  
Type I ◽  
Excitatory Response ◽  
Frequency Responses ◽  
Auditory Responses ◽  
Vocal Signals

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.

scholarly journals Natural echolocation sequences evoke echo-delay selectivity in the auditory midbrain of the FM bat, Eptesicus fuscus

2018 ◽  
Vol 120 (3) ◽  
pp. 1323-1339 ◽  
Author(s):  
Silvio Macías ◽  
Jinhong Luo ◽  
Cynthia F. Moss
Keyword(s):  
Inferior Colliculus ◽  
Sweep Rate ◽  
Eptesicus Fuscus ◽  
Target Range ◽  
Temporal Patterning ◽  
Stimulus Context ◽  
Constant Frequency ◽  
New Findings ◽  
Echo Delay ◽  
Delay Tuning

Echolocating bats must process temporal streams of sonar sounds to represent objects along the range axis. Neuronal echo-delay tuning, the putative mechanism of sonar ranging, has been characterized in the inferior colliculus (IC) of the mustached bat, an insectivorous species that produces echolocation calls consisting of constant frequency and frequency modulated (FM) components, but not in species that use FM signals alone. This raises questions about the mechanisms that give rise to echo-delay tuning in insectivorous bats that use different signal designs. To investigate whether stimulus context may account for species differences in echo-delay selectivity, we characterized single-unit responses in the IC of awake passively listening FM bats, Eptesicus fuscus, to broadcasts of natural sonar call-echo sequences, which contained dynamic changes in signal duration, interval, spectrotemporal structure, and echo-delay. In E. fuscus, neural selectivity to call-echo delay emerges in a population of IC neurons when stimulated with call-echo pairs presented at intervals mimicking those in a natural sonar sequence. To determine whether echo-delay selectivity also depends on the spectrotemporal features of individual sounds within natural sonar sequences, we studied responses to computer-generated echolocation signals that controlled for call interval, duration, bandwidth, sweep rate, and echo-delay. A subpopulation of IC neurons responded selectively to the combination of the spectrotemporal structure of natural call-echo pairs and their temporal patterning within a dynamic sonar sequence. These new findings suggest that the FM bat’s fine control over biosonar signal parameters may modulate IC neuronal selectivity to the dimension of echo-delay. NEW & NOTEWORTHY Echolocating bats perform precise auditory temporal computations to estimate their distance to objects. Here, we report that response selectivity of neurons in the inferior colliculus of a frequency modulated bat to call-echo delay, or target range tuning, depends on the temporal patterning and spectrotemporal features of sound elements in a natural echolocation sequence. We suggest that echo responses to objects at different distances are gated by the bat’s active control over the spectrotemporal patterning of its sonar emissions.

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