scholarly journals Neuropeptide Y expression defines a novel class of GABAergic projection neuron in the inferior colliculus

2019 ◽  
Author(s):  
Marina A. Silveira ◽  
Justin D. Anair ◽  
Nichole L. Beebe ◽  
Pooyan Mirjalili ◽  
Brett R. Schofield ◽  
...  
Keyword(s):  
Neuropeptide Y ◽  
Inferior Colliculus ◽  
Projection Neuron ◽  
Central Nucleus ◽  
Inhibitory Neurons ◽  
Multifaceted Approach ◽  
Functional Roles ◽  
Reporter Mice ◽  
Medial Geniculate ◽  
Whole Cell Recordings

Located in the midbrain, the inferior colliculus (IC) integrates information from numerous auditory nuclei and is an important hub for sound processing. Despite its importance, little is known about the molecular identity and functional roles of defined neuron types in the IC. Using a multifaceted approach in mice, we found that neuropeptide Y (NPY) expression identifies a major class of inhibitory neurons, accounting for approximately one-third of GABAergic neurons in the IC. Retrograde tracing showed that NPY neurons are principal neurons that can project to the medial geniculate nucleus. In brain slice recordings, many NPY neurons fired spontaneously, suggesting that NPY neurons may drive tonic inhibition onto postsynaptic targets. Morphological reconstructions showed that NPY neurons are stellate cells, and the dendrites of NPY neurons in the tonotopically-organized central nucleus of the IC cross isofrequency laminae. Immunostaining confirmed that NPY neurons express NPY, and we therefore hypothesized that NPY signaling regulates activity in the IC. In crosses between Npy1rcre and Ai14 Cre-reporter mice, we found that NPY Y1 receptor (Y1R)-expressing neurons are glutamatergic and were broadly distributed throughout the rostro-caudal extent of the IC. In whole-cell recordings, application of a high affinity Y1R agonist led to hyperpolarization in most Y1R-expressing IC neurons. Thus, NPY neurons represent a novel class of inhibitory principal neurons that are well poised to use GABAergic and NPY signaling to regulate the excitability of circuits in the IC and auditory thalamus.

Auditory Thalamocortical Transmission Is Reliable and Temporally Precise

2005 ◽  
Vol 94 (3) ◽  
pp. 2019-2030 ◽  
Author(s):  
Heather J. Rose ◽  
Raju Metherate
Keyword(s):  
Primary Auditory Cortex ◽  
Inhibitory Neurons ◽  
Latency Variability ◽  
Medial Geniculate ◽  
Low Jitter ◽  
Fast Spiking ◽  
Whole Cell Recordings ◽  
Minimal Stimulation ◽  
Juvenile Mouse

We have used the auditory thalamocortical slice to characterize thalamocortical transmission in primary auditory cortex (ACx) of the juvenile mouse. “Minimal” stimulation was used to activate medial geniculate neurons during whole cell recordings from regular-spiking (RS cells; mostly pyramidal) and fast-spiking (FS, putative inhibitory) neurons in ACx layers 3 and 4. Excitatory postsynaptic potentials (EPSPs) were considered monosynaptic (thalamocortical) if they met three criteria: low onset latency variability (jitter), little change in latency with increased stimulus intensity, and little change in latency during a high-frequency tetanus. Thalamocortical EPSPs were reliable (probability of postsynaptic responses to stimulation was ∼1.0) as well as temporally precise (low jitter). Both RS and FS neurons received thalamocortical input, but EPSPs in FS cells had faster rise times, shorter latencies to peak amplitude, and shorter durations than EPSPs in RS cells. Thalamocortical EPSPs depressed during repetitive stimulation at rates (2–300 Hz) consistent with thalamic spike rates in vivo, but at stimulation rates ≥40 Hz, EPSPs also summed to activate N-methyl-d-aspartate receptors and trigger long-lasting polysynaptic activity. We conclude that thalamic inputs to excitatory and inhibitory neurons in ACx activate reliable and temporally precise monosynaptic EPSPs that in vivo may contribute to the precise timing of acoustic-evoked responses.

Long delay lines for ranging are created by inhibition in the inferior colliculus of the mustached bat

1995 ◽  
Vol 74 (1) ◽  
pp. 1-11 ◽  
Author(s):  
I. Saitoh ◽  
N. Suga
Keyword(s):  
Auditory Cortex ◽  
Receptor Antagonist ◽  
Inferior Colliculus ◽  
Coincidence Detection ◽  
Central Nucleus ◽  
Gamma Aminobutyric Acid ◽  
Delay Lines ◽  
Mustached Bat ◽  
Gabaa Receptor Antagonist ◽  
Medial Geniculate

1. The central auditory system of the mustached bat has arrays of delay-tuned (FM-FM combination-sensitive) neurons in the inferior colliculus, the medial geniculate body, and the auditory cortex. These neurons are tuned to particular echo delays, i.e., target distances. The neural mechanisms for creating the delay-tuned neurons involve delay lines, coincidence detection, and amplification. We have hypothesized that delay lines longer than 4 ms are created by inhibition occurring in the anterolateral division (ALD) of the central nucleus of the inferior colliculus. If this hypothesis is correct, suppression of inhibition occurring in the ALD must shorten the best delays of the collicular, thalamic, and cortical delay-tuned neurons. The aim of the present study is to test this hypothesis. Responses of single delay-tuned neurons in the FM-FM area of the auditory cortex were recorded with a tungsten-wire microelectrode, and the effects of iontophoretic microinjections of strychnine (STR) and/or bicuculline methiodide (BMI) into the ALD were examined on the responses of these neurons. 2. STR (glycine receptor antagonist) and/or BMI [gamma-aminobutyric acid-A (GABAA) receptor antagonist] injections into the ALD shortened the best delays of delay-tuned neurons in the FM-FM area with little change in their response patterns. The longer the best delay of a delay-tuned neuron, the larger the amount of shortening. 3. Inhibition mediated by glycine receptors plays a larger role in creating delay lines than that mediated by GABAA receptors, because STR and BMI, respectively, shortened the best delay of 91 and 74% of the neurons with best delays longer than 4.5 ms. 4. BMI has no effect on the best delays of delay-tuned neurons that were tuned to echo delays shorter than 4.5 ms. 5. The present data support the hypothesis that long delay lines utilized by delay-tuned neurons are created by inhibition occurring in the ALD of the inferior colliculus. However, the amount of shortening in delay lines by STR and/or BMI was generally smaller than that predicted by a neural network model. Therefore the present study partially answers the questions of where and how long delay lines were created.

scholarly journals Antidromic Activation Reveals Tonotopically Organized Projections From Primary Auditory Cortex to the Central Nucleus of the Inferior Colliculus in Guinea Pig

2007 ◽  
Vol 97 (2) ◽  
pp. 1413-1427 ◽  
Author(s):  
Hubert H. Lim ◽  
David J. Anderson
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Spatial Organization ◽  
Medial Geniculate Body ◽  
Primary Auditory Cortex ◽  
Central Nucleus ◽  
Antidromic Activation ◽  
Antidromic Stimulation ◽  
Medial Geniculate ◽  
Layer V

The inferior colliculus (IC) is highly modulated by descending projections from higher auditory and nonauditory centers. Traditionally, corticofugal fibers were believed to project mainly to the extralemniscal IC regions. However, there is some anatomical evidence suggesting that a substantial number of fibers from the primary auditory cortex (A1) project into the IC central nucleus (ICC) and appear to be tonotopically organized. In this study, we used antidromic stimulation combined with other electrophysiological techniques to further investigate the spatial organization of descending fibers from A1 to the ICC in ketamine-anesthetized guinea pigs. Based on our findings, corticofugal fibers originate predominantly from layer V of A1, are amply scattered throughout the ICC and only project to ICC neurons with a similar best frequency (BF). This strict tonotopic pattern suggests that these corticofugal projections are involved with modulating spectral features of sound. Along the isofrequency dimension of the ICC, there appears to be some differences in projection patterns that depend on BF region and possibly isofrequency location within A1 and may be indicative of different descending coding strategies. Furthermore, the success of the antidromic stimulation method in our study demonstrates that it can be used to investigate some of the functional properties associated with corticofugal projections to the ICC as well as to other regions (e.g., medial geniculate body, cochlear nucleus). Such a method can address some of the limitations with current anatomical techniques for studying the auditory corticofugal system.

Delay-Tuned Neurons in the Inferior Colliculus of the Mustached Bat: Implications for Analyses of Target Distance

1999 ◽  
Vol 82 (3) ◽  
pp. 1326-1338 ◽  
Author(s):  
Christine V. Portfors ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Tuning Curve ◽  
Central Nucleus ◽  
Harmonic Frequency ◽  
High Frequency Signal ◽  
Response Properties ◽  
Mustached Bat ◽  
Medial Geniculate ◽  
Higher Harmonic ◽  
Delay Tuning

We examined response properties of delay-tuned neurons in the central nucleus of the inferior colliculus (ICC) of the mustached bat. In the mustached bat, delay-tuned neurons respond best to the combination of the first-harmonic, frequency-modulated (FM1) sweep in the emitted pulse and a higher harmonic frequency-modulated (FM2, FM3 or FM4) component in returning echoes and are referred to as FM-FM neurons. We also examined H1-CF2 neurons. H1-CF2 neurons responded to simultaneous presentation of the first harmonic (H1) in the emitted pulse and the second constant frequency (CF2) component in returning echoes. These neurons served as a comparison as they are thought to encode different features of sonar targets than FM-FM neurons. Only 7% of our neurons (14/198) displayed a single excitatory tuning curve. The rest of the neurons (184) displayed complex responses to sounds in two separate frequency bands. The majority (51%, 101) of neurons were facilitated by the combination of specific components in the mustached bat’s vocalizations. Twenty-five percent showed purely inhibitory interactions. The remaining neurons responded to two separate frequencies, without any facilitation or inhibition. FM-FM neurons (69) were facilitated by the FM1 component in the simulated pulse and a higher harmonic FM component in simulated echoes, provided the high-frequency signal was delayed the appropriate amount. The delay producing maximal facilitation (“best delay”) among FM-FM neurons ranged between 0 and 20 ms, corresponding to target distances ≤3.4 m. Sharpness of delay tuning varied among FM-FM neurons with 50% delay widths between 2 and 13 ms. On average, the facilitated responses of FM-FM neurons were 104% greater than the sum of the responses to the two signals alone. In comparing response properties of delay-tuned, FM-FM neurons in the ICC with those in the medial geniculate body (MGB) from other studies, we find that the range of best delays, sharpness of delay tuning and strength of facilitation are similar in the ICC and MGB. This suggests that by the level of the IC, the basic response properties of FM-FM neurons are established, and they do not undergo extensive transformations with ascending auditory processing.

scholarly journals Neuropeptide Y Expression Defines a Novel Class of GABAergic Projection Neuron in the Inferior Colliculus

2020 ◽  
Vol 40 (24) ◽  
pp. 4685-4699 ◽  
Author(s):  
Marina A. Silveira ◽  
Justin D. Anair ◽  
Nichole L. Beebe ◽  
Pooyan Mirjalili ◽  
Brett R. Schofield ◽  
...  
Keyword(s):  
Neuropeptide Y ◽  
Inferior Colliculus ◽  
Projection Neuron

scholarly journals Transformation of spatial sensitivity along the ascending auditory pathway

2015 ◽  
Vol 113 (9) ◽  
pp. 3098-3111 ◽  
Author(s):  
Justin D. Yao ◽  
Peter Bremen ◽  
John C. Middlebrooks
Keyword(s):  
Inferior Colliculus ◽  
Primary Auditory Cortex ◽  
Noise Burst ◽  
Auditory Pathway ◽  
Sound Level ◽  
Central Nucleus ◽  
Sound Location ◽  
Spatial Sensitivity ◽  
Sound Levels ◽  
Medial Geniculate

Locations of sounds are computed in the central auditory pathway based primarily on differences in sound level and timing at the two ears. In rats, the results of that computation appear in the primary auditory cortex (A1) as exclusively contralateral hemifield spatial sensitivity, with strong responses to sounds contralateral to the recording site, sharp cutoffs across the midline, and weak, sound-level-tolerant responses to ipsilateral sounds. We surveyed the auditory pathway in anesthetized rats to identify the brain level(s) at which level-tolerant spatial sensitivity arises. Noise-burst stimuli were varied in horizontal sound location and in sound level. Neurons in the central nucleus of the inferior colliculus (ICc) displayed contralateral tuning at low sound levels, but tuning was degraded at successively higher sound levels. In contrast, neurons in the nucleus of the brachium of the inferior colliculus (BIN) showed sharp, level-tolerant spatial sensitivity. The ventral division of the medial geniculate body (MGBv) contained two discrete neural populations, one showing broad sensitivity like the ICc and one showing sharp sensitivity like A1. Dorsal, medial, and shell regions of the MGB showed fairly sharp spatial sensitivity, likely reflecting inputs from A1 and/or the BIN. The results demonstrate two parallel brainstem pathways for spatial hearing. The tectal pathway, in which sharp, level-tolerant spatial sensitivity arises between ICc and BIN, projects to the superior colliculus and could support reflexive orientation to sounds. The lemniscal pathway, in which such sensitivity arises between ICc and the MGBv, projects to the forebrain to support perception of sound location.

Single-Unit Responses in the Inferior Colliculus of Decerebrate Cats II. Sensitivity to Interaural Level Differences

1999 ◽  
Vol 82 (1) ◽  
pp. 164-175 ◽  
Author(s):  
Kevin A. Davis ◽  
Ramnarayan Ramachandran ◽  
Bradford J. May
Keyword(s):  
Frequency Response ◽  
Inferior Colliculus ◽  
Free Field ◽  
Central Nucleus ◽  
Type I ◽  
Discharge Rates ◽  
Ipsilateral Stimulation ◽  
Interaural Level Differences ◽  
Type V ◽  
Decerebrate Cats

Single units in the central nucleus of the inferior colliculus (ICC) of unanesthetized decerebrate cats can be grouped into three distinct types (V, I, and O) according to the patterns of excitation and inhibition revealed in contralateral frequency response maps. This study extends the description of these response types by assessing their ipsilateral and binaural response map properties. Here the nature of ipsilateral inputs is evaluated directly using frequency response maps and compared with results obtained from methods that rely on sensitivity to interaural level differences (ILDs). In general, there is a one-to-one correspondence between observed ipsilateral input characteristics and those inferred from ILD manipulations. Type V units receive ipsilateral excitation and show binaural facilitation (EE properties); type I and type O units receive ipsilateral inhibition and show binaural excitatory/inhibitory (EI) interactions. Analyses of binaural frequency response maps show that these ILD effects extend over the entire receptive field of ICC units. Thus the range of frequencies that elicits excitation from type V units is expanded with increasing levels of ipsilateral stimulation, whereas the excitatory bandwidth of type I and O units decreases under the same binaural conditions. For the majority of ICC units, application of bicuculline, an antagonist for GABAA-mediated inhibition, does not alter the basic effects of binaural stimulation; rather, it primarily increases spontaneous and maximum discharge rates. These results support our previous interpretations of the putative dominant inputs to ICC response types and have important implications for midbrain processing of competing free-field sounds that reach the listener with different directional signatures.

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