Multiple Components of Ipsilaterally Evoked Inhibition in the Inferior Colliculus

1999 ◽  
Vol 82 (2) ◽  
pp. 593-610 ◽  
Author(s):  
Achim Klug ◽  
Eric E. Bauer ◽  
George D. Pollak
Keyword(s):  
Inferior Colliculus ◽  
Background Activity ◽  
Spike Count ◽  
Central Nucleus ◽  
Initial Portion ◽  
Multiple Components ◽  
Iontophoretic Application ◽  
Excitatory Neurotransmitters ◽  
Contralateral Ear ◽  
Stimulation Of

The central nucleus of the inferior colliculus (ICc) receives a large number of convergent inputs that are both excitatory and inhibitory. Although excitatory inputs typically are evoked by stimulation of the contralateral ear, inhibitory inputs can be recruited by either ear. Here we evaluate ipsilaterally evoked inhibition in single ICc cells in awake Mexican free-tailed bats. The principal question we addressed concerns the degree to which ipsilateral inhibition at the ICc suppresses contralaterally evoked discharges and thus creates the excitatory-inhibitory (EI) properties of ICc neurons. To study ipsilaterally evoked inhibition, we iontophoretically applied excitatory neurotransmitters and visualized the ipsilateral inhibition as a gap in the carpet of background activity evoked by the transmitters. Ipsilateral inhibition was seen in 86% of ICc cells. The inhibition in most cells had both glycinergic and GABAergic components that could be blocked by the iontophoretic application of bicuculline and strychnine. In 80% of the cells that were inhibited, the ipsilateral inhibition and contralateral excitation were temporally coincident. In many of these cells, the ipsilateral inhibition suppressed contralateral discharges and thus generated the cell’s EI property in the ICc. In other cells, the ipsilateral inhibition was coincident with the initial portion of the excitation, but the inhibition was only 2–4 ms in duration and suppressed only the first few contralaterally evoked discharges. The suppression was so slight that it often could not be detected as a decrease in the spike count generated by increasing ipsilateral intensities. Twenty percent of the cells that expressed inhibition, however, had inhibitory latencies that were longer than the excitatory latencies. In these neurons, the inhibition arrived too late to suppress most or any of the discharges. Finally, in the majority of cells, the ipsilateral inhibition persisted for tens of milliseconds beyond the duration of the signal that evoked it. Thus ipsilateral inhibition has multiple components and one or more of these components are typically evoked in ICc neurons by sound received at the ipsilateral ear.

Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat

1995 ◽  
Vol 74 (4) ◽  
pp. 1701-1713 ◽  
Author(s):  
A. Klug ◽  
T. J. Park ◽  
G. D. Pollak
Keyword(s):  
Receptor Antagonist ◽  
Inferior Colliculus ◽  
Spike Count ◽  
Gabaergic Inhibition ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Contralateral Ear ◽  
Glycinergic Inhibition ◽  
Ipsilateral Stimulation ◽  
Stimulation Of

1. The mammalian inferior colliculus contains large populations of binaural cells that are excited by stimulation of the contralateral ear and are inhibited by stimulation of the ipsilateral ear, and are called excitatory/inhibitory (EI) cells. Neurons with EI properties are initially created in the lateral superior olive (LSO), which, in turn, sends strong bilateral projections to the inferior colliculus. The questions that we address in this report are 1) whether the inhibition evoked by stimulation of the ipsilateral ear occurs at the inferior colliculus or whether it occurs in a lower nucleus, presumably the LSO; and 2) if the ipsilaterally evoked inhibition occurs at the inferior colliculus, is the inhibition a consequence of glycinergic innervation or is it a consequence of GABAergic innervation. To study these questions, we recorded from 61 EI neurons in the inferior colliculus of the mustache bat before and during the iontophoretic application of the glycine receptor antagonist, strychnine. We also tested the effects of the gamma-aminobutyric acid-A (GABAA) receptor antagonist, bicuculline, on 38 of the 61 neurons that were tested with strychnine. The main finding is that glycinergic or GABAergic inhibition, or both, contribute to the ipsilaterally evoked inhibition in approximately 50% of the EI neurons in the inferior colliculus. 2. Strychnine and bicuculline had different effects on the magnitude of the spike counts evoked by stimulation of the contralateral (excitatory) ear. On average, strychnine caused the maximum spike count evoked by contralateral stimulation to increase by only 23%. The relatively small effects of strychnine on response magnitude are in marked contrast to the effects of bicuculline, which usually caused much larger increases in spike counts. For example, although strychnine caused spike counts to more than double in approximately 25% of the collicular neurons, bicuculline caused a doubling of the spike count in approximately 60% of the cells. 3. The inhibitory influences of ipsilateral stimulation were evaluated by driving the neurons with a fixed intensity at the contralateral ear and then documenting the reductions in spike counts due to the presentation of progressively higher intensities at the ipsilateral ear. In 64% of the neurons sampled, blocking glycinergic inhibition with strychnine had little or no effect on the ipsilaterally evoked inhibition. These cells remained as strongly inhibited during the application of strychnine as they did before its application. In addition, the ipsilateral intensity that produced complete or nearly complete spike suppression in the predrug condition was also unchanged by strychnine. 4. In 36% of the neurons, strychnine markedly reduced the degree of ipsilaterally evoked spike suppression. In five of these neurons, there was a complete elimination of the ipsilateral inhibition: these neurons were transformed from strongly inhibited EI neurons into monaural neurons. 5. The influence of both strychnine and bicuculline was tested sequentially in 38 neurons. In about one-half of these cells, (53%, 20/38) the ipsilaterally evoked inhibition was unaffected by either drug. In 10 other units (26%), both drugs substantially reduced or eliminated the ipsilaterally evoked inhibition. In most of these cells, both bicuculline and strychnine reduced the ipsilaterally evoked inhibition to a similar degree. In the remaining eight cells studied with both drugs (21%), the ipsilaterally evoked inhibition was reduced or eliminated by one of the drugs, but not by both. 6. These results show that both glycinergic and GABAergic projections influence the ipsilaterally evoked inhibition in about one-half of the EI neurons in the inferior colliculus. The glycinergic inhibition elicited by ipsilateral stimulation is most likely due to projections from the ipsilateral lateral superior olive, whereas the GABAergic inhibition evoked by ipsilateral stimulation is most likely caused b

The roles of GABAergic and glycinergic inhibition on binaural processing in the dorsal nucleus of the lateral lemniscus of the mustache bat

1994 ◽  
Vol 71 (6) ◽  
pp. 1999-2013 ◽  
Author(s):  
L. Yang ◽  
G. D. Pollak
Keyword(s):  
Tone Burst ◽  
Gabaergic Inhibition ◽  
Gamma Aminobutyric Acid ◽  
Lateral Lemniscus ◽  
Dorsal Nucleus ◽  
Iontophoretic Application ◽  
Monaural Stimulation ◽  
Contralateral Ear ◽  
Glycinergic Inhibition ◽  
Stimulation Of

1. We studied the monaural and binaural response properties of 99 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat before and during the iontophoretic application of antagonists that blocked gamma-aminobutyric acid-A (GABAA) receptors (bicuculline) or glycine receptors (strychnine). All cells were driven by monaural stimulation of the contralateral ear, whereas monaural stimulation of the ipsilateral ear never evoked discharges. The binaural properties of 81 neurons were determined by holding the intensity constant at the contralateral ear and presenting a variety of intensities to the ipsilateral ear. This procedure generated interaural intensity disparity (IID) functions and allowed us to determine the effect of ipsilaterally evoked inhibition on a constant excitatory drive evoked by the contralateral ear. 2. One of the main findings is that the IID functions in the majority of DNLL neurons were not affected by application of either strychnine or bicuculline. Blocking glycinergic inhibition with strychnine had no effect on the IID functions in 75% of the cells studied. However, strychnine did change the IID functions in approximately 25% of the DNLL population. In those cells glycinergic inhibition appeared to be partially, or, in a few cases, entirely responsible for the ipsilaterally evoked spike suppression. In contrast, blocking GABAergic inhibition with bicuculline had no discernible effect on the ipsilaterally evoked spike suppression in any of the excitatory/inhibitory cells that we recorded. GABAergic inhibition, therefore, plays no role in the formation of IID functions of neurons in the DNLL. Furthermore, the results suggest that glycinergic inhibition also does not contribute to the suppression of spikes evoked by stimulation of the contralateral ear in the vast majority of DNLL neurons. 3. Although the majority of IID functions were not influenced when either GABAergic or glycinergic innervation was blocked, ipsilateral stimulation alone evoked both a glycinergic and GABAergic inhibition in most DNLL cells. These inhibitory events were demonstrated in 18 other cells by evoking discharges with the iontophoretic application of glutamate. Stimulating the ipsilateral ear alone under these conditions caused a suppression of the glutamate-evoked discharges. Furthermore, the spike suppression persisted for a period of time that was longer than the duration of the tone burst at the ipsilateral ear. 4. The application of bicuculline or strychnine had different effects on the glutamate-elicited spikes. Bicuculline reduced the duration of the inhibition, and it was always the latter portion of the inhibition that was abolished by bicuculline. In more than half of the cells studied strychnine also reduced the duration of the inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

Responses of neurons in the cat's superior colliculus to acoustic stimuli. I. Monaural and binaural response properties

1985 ◽  
Vol 53 (3) ◽  
pp. 726-745 ◽  
Author(s):  
J. A. Hirsch ◽  
J. C. Chan ◽  
T. C. Yin
Keyword(s):  
Superior Colliculus ◽  
Characteristic Frequency ◽  
Spike Count ◽  
Threshold Intensity ◽  
Interaural Time Differences ◽  
Average Characteristic ◽  
Stimulus Interval ◽  
The Mean ◽  
Contralateral Ear ◽  
Stimulation Of

Using extracellular electrodes we studied acoustic responses in the superior colliculus (SC) of the barbiturate-anesthetized cat. Pure tonal stimuli were delivered through sealed and calibrated earphones and were presented either monaurally or binaurally with interaural intensity differences (IIDs) and interaural time differences (ITDs). Acoustically sensitive cells were found in the intermediate and deep layers of the SC throughout its rostrocaudal and mediolateral extent. Most cells (80%) discharged only at stimulus onset; the rest had more complex firing patterns. For 88% of our sample the mean first-spike latency measured at 20 dB above threshold ranged between 6 and 16 ms. The sharpness and threshold intensity of the frequency tuning curves varied widely. In the SC, the average characteristic frequency and threshold intensity were higher than in other auditory brain stem nuclei. Neurons whose characteristic frequency was low were never sharply tuned. The probability of response decreased when the repetition rate at which the stimuli were delivered increased. The mean stimulus interval at which spike count reached 50% of maximum was 360 ms. Most (83%) of the cells discharged only to monaural stimulation of the contralateral ear, 7% responded to tones applied to either ear and only 1% to only ipsilateral input. The remaining cells responded only to stimulation of both ears. With binaural stimuli, most neurons (80%) could be shown to receive input from both ears. Seventy percent of the binaural cells showed predominant binaural inhibition (BI), 25% binaural facilitation (BF), and 5% a more complex mixture. Because the majority of SC neurons had high characteristic frequencies, we examined their responses to IIDs. The spike count vs. IID functions of BI cells were monotonic and sigmoidal, those of BF cells were nonmonotonic and bell-shaped. The slopes and horizontal positions of the curves varied among neurons. IIDs favoring the contralateral ear were the most effective. For a given cell, increasing the mean binaural level extended the range of IIDs that evoked maximal discharge. A small number of cells was sensitive to physiologically significant interaural time differences of low-frequency tones or the envelopes of amplitude-modulated, high-frequency tones.

scholarly journals A function for binaural integration in auditory grouping and segregation in the inferior colliculus

2015 ◽  
Vol 113 (6) ◽  
pp. 1819-1830 ◽  
Author(s):  
Kyle T. Nakamoto ◽  
Trevor M. Shackleton ◽  
David A. Magezi ◽  
Alan R. Palmer
Keyword(s):  
Inferior Colliculus ◽  
Central Nucleus ◽  
Harmonic Complex ◽  
Auditory Grouping ◽  
Sound Segregation ◽  
Fundamental Frequencies ◽  
Complex Stimuli ◽  
Left And Right ◽  
Contralateral Ear ◽  
Contralateral Stimulus

Responses of neurons to binaural, harmonic complex stimuli in urethane-anesthetized guinea pig inferior colliculus (IC) are reported. To assess the binaural integration of harmonicity cues for sound segregation and grouping, responses were measured to harmonic complexes with different fundamental frequencies presented to each ear. Simultaneously gated harmonic stimuli with fundamental frequencies of 125 Hz and 145 Hz were presented to the left and right ears, respectively, and recordings made from 96 neurons with characteristic frequencies >2 kHz in the central nucleus of the IC. Of these units, 70 responded continuously throughout the stimulus and were excited by the stimulus at the contralateral ear. The stimulus at the ipsilateral ear excited (EE: 14%; 10/70), inhibited (EI: 33%; 23/70), or had no significant effect (EO: 53%; 37/70), defined by the effect on firing rate. The neurons phase locked to the temporal envelope at each ear to varying degrees depending on signal level. Many of the cells (predominantly EO) were dominated by the response to the contralateral stimulus. Another group (predominantly EI) synchronized to the contralateral stimulus and were suppressed by the ipsilateral stimulus in a phasic manner. A third group synchronized to the stimuli at both ears (predominantly EE). Finally, a group only responded when the waveform peaks from each ear coincided. We conclude that these groups of neurons represent different “streams” of information but exhibit modifications of the response rather than encoding a feature of the stimulus, like pitch.

Interaural Level Difference Processing in the Lateral Superior Olive and the Inferior Colliculus

2004 ◽  
Vol 92 (1) ◽  
pp. 289-301 ◽  
Author(s):  
Thomas J. Park ◽  
Achim Klug ◽  
Michael Holinstat ◽  
Benedikt Grothe
Keyword(s):  
Inferior Colliculus ◽  
Population Analysis ◽  
Single Cells ◽  
Central Nucleus ◽  
Interaural Level Difference ◽  
Population Activity ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Synaptic Level ◽  
Stimulation Of

Interaural level differences (ILDs) provide salient cues for localizing high-frequency sounds in space, and populations of neurons that are sensitive to ILDs are found at almost every synaptic level from brain stem to cortex. These cells are predominantly excited by stimulation of one ear and predominantly inhibited by stimulation of the other ear, such that the magnitude of their response is determined in large part by the intensities at the 2 ears. However, in many cases ILD sensitivity is also influenced by overall intensity, which challenges the idea of unambiguous ILD coding. We investigated whether ambiguity is reduced from one synaptic level to another for 2 centers in the so-called ILD processing pathway. We recorded from single cells in the free-tailed bat lateral superior olive (LSO), the first station where ILDs are coded, and the central nucleus of the inferior colliculus (ICC), which receives a strong projection from the LSO, as well as convergent projections from many other auditory centers. We assessed effects of overall intensity by comparing ILD functions generated with different fixed intensities to the excitatory ear. LSO cells were characterized by functions that shifted in a systematic manner with increasing intensity to the excitatory ear. In contrast, significantly more ICC cells had functions that were stable across overall sound intensity, indicating that hierarchical transformations increase stability. Furthermore, a population analysis based on proportion of active cells indicated that stability in the ICC was greatly enhanced when overall population activity was considered.

External nucleus of inferior colliculus: auditory and spinal somatosensory afferents and their interactions

1978 ◽  
Vol 41 (4) ◽  
pp. 837-847 ◽  
Author(s):  
L. M. Aitkin ◽  
H. Dickhaus ◽  
W. Schult ◽  
M. Zimmermann
Keyword(s):  
Inferior Colliculus ◽  
Pure Tone ◽  
Tactile Stimulation ◽  
Receptive Fields ◽  
The Body ◽  
Central Nucleus ◽  
Auditory Input ◽  
Somatosensory Information ◽  
Somatic Receptive Fields ◽  
Stimulation Of

1. The discharges of 129 units were studied in the external nucleus of the inferior colliculus of 11 anesthetised and paralyzed cats. This region is known to receive fibers from auditory nuclei and the dorsal column nuclei. 2. Stimuli used were pure tone bursts, monaural or binaural, tactile stimulation of the body surface, and electrical stimulation of the dorsal columns (DC) at a low cervical level and of the contralateral and ipsilateral tibial nerves. 3. Forty-six percent of units were only influenced by one type of stimulation (26% auditory, 20% DC). Of the remaining bimodally influenced units, the majority was excited by pure tone stimuli and inhibited by DC stimulation. 4. A small proportion of the total population (18%) was excited by both DC and auditory input, and units sensitive to both tones and tactile stimulation of the skin were rare (4%). 5. Auditory tuning curves were generally very broad compared with those of units in the central nucleus of the inferior colliculus. Similarly, somatic receptive fields were large and usually extended over a whole limb. 6. The majority of tone-responsive units were influenced binaurally (70%); most somatic receptive fields were located on the contralateral fore- or hindlimb (16/18). 7. The results indicate that both auditory and somatosensory information is contained in the discharges of units in the external nucleus of the inferior colliculus. 8. Speculations are made about the role of this nucleus in descending auditory input to the spinal cord and in the comparison of auditory and cutaneous information during sound-evoked coordinated body movements.

Response Properties of Neurons in the Inferior Colliculus of the Monaurally Deafened Ferret to Acoustic Stimulation of the Intact Ear

1997 ◽  
Vol 78 (2) ◽  
pp. 767-779 ◽  
Author(s):  
David McAlpine ◽  
Russell L. Martin ◽  
Jennifer E. Mossop ◽  
David R. Moore
Keyword(s):  
Inferior Colliculus ◽  
Single Unit ◽  
Acoustic Stimulation ◽  
Analysis Of Covariance ◽  
Central Nucleus ◽  
Spontaneous Discharge ◽  
Response Properties ◽  
Ipsilateral Stimulation ◽  
Intensity Functions ◽  
Stimulation Of

McAlpine, David, Russell L. Martin, Jennifer E. Mossop, and David R. Moore. Response properties of neurons in the inferior colliculus of the monaurally deafened ferret to acoustic stimulation of the intact ear. J. Neurophysiol. 78: 767–779, 1997. Response properties of neurons in the central nucleus of the inferior colliculus (ICC) were investigated after unilateral cochlear removal at various ages during infancy. Nineteen ferrets had the right cochlea surgically ablated, either in adulthood or on postnatal day (P) 5, 25, or 40, 3–18 mo before recording. Adult ablations were made on the same day as (“acute,” n = 3), or 2–3 mo before (“chronic,” n = 3), recording. Two ferrets were left binaurally intact. Single-unit ( n = 702) and multiunit ( n = 1,819) recordings were made in the ICC of barbiturate-anesthetized ferrets ipsilateral (all ages) or contralateral (P5 and acute adult only) to the intact ear. In binaurally intact animals, tonal stimulation of the contralateral ear evoked excitatory activity at the majority (94%) of recording loci, whereas stimulation of the ipsilateral ear evoked activity at only 33% of recording loci. In acutely ablated animals, the majority of contralateral (90%) and ipsilateral (70%) loci were excited by tonal stimulation of the intact ear. In chronically ablated animals, 80–90% of loci were excited by ipsilateral stimulation. Single-unit thresholds were generally higher for low-best frequency (BF) than for high-BF units, and higher in the ipsilateral than in the contralateral ICC. Analysis of covariance showed highly significant differences between all of the ipsilateral and contralateral groups, but no effects of age at ablation or survival time following ablation, other than that the group ablated at P25 had higher mean ipsilateral thresholds than the groups ablated at P5 or, acutely, in adulthood. Cochlear ablation at P5, 25, or 40 resulted in a significant increase in dynamic ranges of ipsilateral ICC unit rate-intensity functions relative to acutely ablated animals. Dynamic ranges of units in the contralateral ICC of P5-ablated ferrets were also significantly increased compared with those of acutely ablated animals. Cochlear ablation at P5, 25, or 40 resulted in a significant increase in single-unit spontaneous discharge rates in the ICC ipsilateral but not contralateral (P5 only) to the intact ear. These data show that unilateral cochlear removal in adult ferrets leads to a rapid and dramatic increase in the proportion of neurons in the ICC ipsilateral to the intact ear that is excited by acoustic stimulation of that ear. In addition, the data confirm that, in ferrets, cochlear removal in infancy leads to a further increase in responsiveness of individual neurons in the ipsilateral ICC. Finally, the data show that responses in the ICC contralateral to the intact ear are largely but not completely unchanged by unilateral cochlear removal.

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