GABA and Glycine Inputs Control Discharge Rate within the Excitatory Response Area of Primary-Like and Phase-Locked AVCN Neurons

1993 ◽  
pp. 239-252 ◽  
Author(s):  
Donald M. Caspary ◽  
Peggy S. Palombi ◽  
Patricia M. Backoff ◽  
Robert H. Helfert ◽  
Paul G. Finlayson
1994 ◽  
Vol 72 (5) ◽  
pp. 2124-2133 ◽  
Author(s):  
D. M. Caspary ◽  
P. M. Backoff ◽  
P. G. Finlayson ◽  
P. S. Palombi

1. The amino acid neurotransmitters gamma-aminobutyric acid (GABA) and glycine function as inhibitory neurotransmitters associated with nonprimary inputs onto spherical bushy and stellate cells, two principal cell types located in the anteroventral cochlear nucleus (AVCN). These neurons are characterized by primary-like (including phase-locked) and chopper temporal response patterns, respectively. 2. Inhibition directly adjacent to the excitatory response area has been hypothesized to sharpen or limit the breadth of the tonal frequency receptive field. This study was undertaken to test whether GABA and glycine circuits function primarily to sharpen the lateral edges of the tonal excitatory response area or to modulate discharge rate within central portions of the excitatory response area of AVCN neurons. 3. To test this, iontophoretic application of the glycineI antagonist, strychnine, or the GABAA antagonist, bicuculline, was used to block inhibitory inputs after obtaining control families of isointensity contours (response areas) from extracellularly recorded AVCN neurons. 4. Blockade of GABA and/or glycine inputs was found to increase discharge rate primarily within the excitatory response area of neurons displaying chopper and primary-like temporal responses with little or no change in bandwidth or in off-characteristic frequency (CF) discharge rate. 5. The principal sources of inhibitory inputs onto AVCN neurons are cells located in the dorsal cochlear nucleus and superior olivary complex, which appear to be tonotopically matched to their targets. In agreement with these morphological studies, the data presented in this paper suggest that most GABA and/or glycine inhibition is tonotopically aligned with excitatory inputs. 6. These findings support models that suggest that GABA and/or glycine inputs onto AVCN neurons are involved in circuits that adjust gain to enable the detection of signals in noise by enhancing signal relative to background.


1996 ◽  
Vol 75 (6) ◽  
pp. 2211-2219 ◽  
Author(s):  
P. S. Palombi ◽  
D. M. Caspary

1. Recent studies have suggested that gamma-aminobutyric acid (GABA) inputs shape monaural and binaural neuronal response properties in the central nucleus of the inferior colliculus (CIC). CIC neurons receive major inhibitory GABAergic projections from intrinsic, commissural, and extrinsic sources. Many GABAergic projections now are thought to arise from cells that are tonotopically matched to their CIC targets. 2. We tested the hypothesis that GABA circuits are aligned primarily within the CIC target neuron's excitatory response area and therefore have their greatest effects on discharge rate mainly within that frequency domain. GABA inhibition was examined by recording families of isointensity contours before, during, and after GABAA receptor blockade. Iontophoretic application of bicuculline-methiodide (BMI) was used to block GABAA receptors. Quantitative measures of frequency bandwidth and z-score analysis of discharge rate within the excitatory receptive field were used to compare pre- and postdrug conditions. 3. Chinchilla CIC unit response properties were similar to those described for other species, with a high percentage of phasic temporal response patterns and nonmonotonic rate-intensity functions in response to monaural contralateral characteristic frequency (CF) tones. Binaural responses of most CIC neurons showed suppression of contralaterally evoked responses by ipsilateral stimulation. 4. For 85% of CIC neurons, blockade of GABAA inputs was found to increase discharge rate within the excitatory response area. Forty-five percent were classified as near-CF changes and 32% as near-CF and low side. Changes in lateral/flanking inhibition in the absence of near-CF changes were never observed. Forty-one percent of CIC neurons displayed less than a 10% increase in frequency bandwidth at 25-35 dB above threshold with BMI application. 5. These data suggest that GABA inhibition arises primarily from neurons with inhibitory fields aligned with their CIC targets. Thus the effect of the inhibition is primarily contained within or overlapping each target neuron's excitatory response area. CIC GABAergic circuits may function to adjust the gain needed for coding complex signals over a wide dynamic range.


1995 ◽  
Vol 73 (5) ◽  
pp. 1876-1891 ◽  
Author(s):  
M. B. Calford ◽  
M. N. Semple

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)


1976 ◽  
Vol 39 (1) ◽  
pp. 162-178 ◽  
Author(s):  
R. Britt ◽  
A. Starr

Unitary discharge patterns (peristimulus time histograms or PSTH) and synaptic events were studies with intracellular recording techniques in 164 cat cochlear nucleus cells to steady-frequency tone bursts 250 ms in duration. There were four response types defined on the basis of the shape of the discharge patterns to tones at the characteristic or best frequency. Primarylike units resemble eighth nerve fibres and have a maximum discharge at tone onset, followed by a smooth decline to a steady level of activity. Buildup units have a transient response at tone onset, followed a period of little or not activity before gradually increasing their discharge rate for the remainder of the tone burst. Onset units have an initial burst of spikes at the onset, with little or no activity for the remainder of the tone burst. Pause units have a long latency (10-30 ms) between tone onset and the appearance of low levels of unit activity, which then gradually increase in rate for the remainder of the tone burst. Changes in signal frequency or intensity within the excitatory response area did not modify response patterns of primarylike and onset units, but could evoke primarylike patterns in buildup and pause units. Inhibition manifested by suppression of spontaneous activity and membrane hyperpolarization were of three kinds: 1) in response to signals at the edges of the excitatory response area (i.e., the inhibitory surround) and detected in onset buildup, and pause units but not in primarylike units; 2) occurring at the offset of tones in the excitatory response area and detected in all four types of cochlear nucleus cells; 3) during excitatory tone bursts in onset and buildup units associated with the periods of suppressed unit activity. Membrane hyperpolarization did not accompany the delay in unit activity after tone onset in pause units. Inhibitory events in cochlear nucleus cells provide mechanisms for producing diversity in the temporal pattern of discharges to acoustic signals which may underly the encoding of complex features of sounds.


1992 ◽  
Vol 67 (3) ◽  
pp. 738-746 ◽  
Author(s):  
P. S. Palombi ◽  
D. M. Caspary

1. The role of GABAergic inhibitory inputs onto posteroventral cochlear nucleus (PVCN) neurons in the anesthetized chinchilla was investigated through iontophoretic application of the GABAA receptor agonist muscimol and the GABAA receptor antagonist bicuculline. The majority of the neurons studied displayed phasic temporal response patterns. 2. All the neurons were sensitive to bicuculline and displayed an increase in discharge rate, which was greatest during the post-onset portion of the response. Most of the tested neurons were also sensitive to muscimol, which appeared to mimic the putative effect of endogenous GABA. 3. Bicuculline reduced the average first-spike latency and the average variability of the first-spike latency. Muscimol had the opposite effect. 4. Bicuculline did not significantly alter the threshold but rather increased discharge rate at suprathreshold intensities. 5. The width of the excitatory response area was not significantly increased by application of bicuculline. The increase in discharge rate occurred within the units' excitatory response areas. 6. The shape of the rate-intensity functions was not altered by bicuculline application. 7. We conclude that GABAergic inhibitory inputs control the post-onset discharge rate of some PVCN neurons. They may suppress tonic activity, resulting in more phasic discharge patterns.


1996 ◽  
Vol 75 (1) ◽  
pp. 171-183 ◽  
Author(s):  
J. Wang ◽  
R. J. Salvi ◽  
N. Powers

1. The discharge patterns of 40 neurons in the central nucleus of the inferior colliculus (ICC) of the chinchilla were evaluated before and after acute cochlea trauma from intense tone exposure. Single-unit recordings were obtained from neurons in the ICC contralateral to the sound-stimulated ear. Cochlear trauma was induced with a short-duration (15-25 min), high-intensity pure tone (95-115 dB SPL) at a frequency above the neuron's characteristic frequency (CF). The aim of the traumatizing exposure was to damage the peripheral sensory receptors associated with frequencies above the neuron's CF. The damage was expected to attenuate inputs to the neural circuits responsible for activating the inhibitory sidebands above CF. 2. Three types of frequency-threshold tuning curves were observed before the exposure: 1) open V tuning curves (55%) that became wider as sound intensity increased; 2) level-tolerant tuning curves (37.5%) that maintained a very narrow bandwidth even at high sound intensities; and 3) upper-threshold tuning curves (7.5%) in which excitatory responses were elicited at low and moderate intensities, but not at high intensities. The traumatizing exposure caused a dramatic widening of level-tolerant (80% of sample) and upper-threshold tuning curves (100% of sample) at high sound intensities but caused almost no change in the low-threshold tip of the tuning curves. By contrast, tuning curves with an open V configuration were generally unaffected (approximately 90% of sample) by the traumatizing exposure. 3. Discharge rate-level functions in the ICC were of two general types: 1) strongly nonmonotonic (60%) or 2) saturating, monotonic (40%). The traumatizing exposure caused a significant increase in the suprathreshold discharge rates in 70% of all neurons studied. Among the neurons with strongly nonmonotonic discharge rate-level functions, 93% showed a significant increase in discharge rate. 4. The poststimulus time histograms (PSTH) to tone bursts were of three main types: 1) onset, 2) pauser, and 3) sustained responders. The traumatizing exposure had almost no effect on the PSTH of onset or sustained responders. However, pause PSTH frequently (75%) showed a significant decrease in the pause duration and an increase in the sustained discharge rate following the pause after the exposure. 5. The results suggest that the response properties of neurons with extremely narrow tuning curves and nonmonotonic discharge rate-level functions are shaped by an inhibitory circuit that is activated by frequencies above the high-frequency flank of the tuning curve. This inhibitory circuit modifies the excitatory response in the following ways: 1) it narrows the excitatory response area at suprathreshold intensities particularly at frequencies below CF, 2) it alters the shape of the discharge rate-level function by suppressing the discharge rates at suprathreshold intensities, and 3) it modifies the temporal discharge pattern of the pause PSTH by suppressing neural activity that occurs after the onset response. The effects of these inhibitory inputs can be reduced (disinhibition) by damaging the sensory cells in the inner ear that activate this circuit. The exact locus of the inhibitory circuit(s) is unknown but may involve inhibitory inputs located at the level of the cochlear nucleus and/or at levels up to the inferior colliculus.


1996 ◽  
Vol 75 (2) ◽  
pp. 780-794 ◽  
Author(s):  
A. R. Palmer ◽  
D. Jiang ◽  
D. H. Marshall

1. The responses of units in the ventral cochlear nucleus in anesthetized guinea pigs have been measured to best-frequency tones, noise bands geometrically centered around the unit best frequency, and noise bands asymmetrically positioned around the best frequency. 2. Each unit isolated was characterized using peristimulus time histograms (PSTHs) to best-frequency tones at 20 and 50 dB suprathreshold, frequency-intensity response areas and rate-versus-level functions in response to best-frequency tones and wideband noise. The data reported here are derived from full analyses of 5 chopper units and 17 onset units. The onsets were divided into onset-I (OnI), onset-L (OnL), and onset-C (OnC) by the criteria described by Winter and Palmer: the PSTHs of OnI units show only an onset response, OnL units respond with a single spike at onset followed by a low level of sustained activity, and OnC units have PSTHs with one to four onset peaks and low levels of sustained discharge. 3. In response to geometrically centered noise bands of constant spectral density, the discharge of chopper units and one OnI unit increased over a relatively narrow range of bandwidths, corresponding to the equivalent rectangular bandwidth calculated from their response area, and then became constant. In contrast, OnL and OnC units showed increases in discharge rate with noise bandwidth over very wide ranges of bandwidth. The growth of the discharge rate with noise bandwidth was approximately linear on double logarithmic axes and therefore could be described by a power function with an exponent of 0.37. This relation held even for noise levels near threshold. 4. When noise bands with constant spectral density (at the input to the earphone) were presented with one edge fixed at the unit's best frequency, the discharge rate of most chopper units and the one OnI unit increased over a narrow range of bandwidths and then became constant. This pattern was observed irrespective of whether the second edge of the noise was progressively increased above, or decreased below, the best frequency. For two of the chopper units, in which lateral inhibitory sidebands could be demonstrated, increasing the noise bandwidth led first to increases and then to decreases in the discharge rate as the noise energy impinged upon the sideband. The chopper units act like energy detectors with a filter corresponding to their single tone response area, but, for some units, with the addition of inhibitory sidebands. 5. For the OnL and OnC units, increasing the noise bandwidth above or below best frequency caused progressive increases in the discharge rate over wide ranges of bandwidth. These increases occurred even for low noise spectral densities. The growth in discharge rate for these onset units was well fitted at all spectral density levels by power functions: one above best frequency and one below. At levels of the noise 40 dB above the unit threshold, the point at which the discharge rate reached 90% of its maximum was, on average, about 2 octaves below best frequency and 1 octave above. For some onset units, changes in the discharge rate were seen as the noise bandwidth was varied over about 14 kHz, which is about one-third of the total frequency hearing range of the guinea pig. 6. The data for onset units is consistent with the hypothesis that onset units in the ventral cochlear nucleus achieve their precision in the temporal domain by integration of the inputs from auditory nerve fibers with a wide range of best frequencies. The range of frequency over which onset units integrate frequency matches that of the inhibitory input to dorsal cochlear nucleus neurons, suggesting a possible role as an inhibitory interneuron.


1988 ◽  
Vol 23 (4) ◽  
pp. 568-577
Author(s):  
Harold S. Bailey

Abstract The water quality of the upper 110 kilometres of the St. Croix River is considered to be pristine. A major industrial discharge renders the lower 14 kilometres of the river a water quality limited segment. Prior to 1970 the Georgia-Pacific Pulp and Paper Mill at Woodland, Maine, discharged untreated effluent directly into the river causing dissolved oxygen concentrations to drop well below 5 mg/L, the objective chosen in the interest of restoring endemic fish populations. Since 1972, the Mill has installed primary and secondary treatment, regulated river discharge rate and effluent composition which has greatly improved the summer dissolved oxygen regime. By 1980, dissolved oxygen concentrations were generally above 5.0 mg/L and restocking the river with Atlantic Salmon (Salmo salar) was initiated.


2005 ◽  
Vol 94 (4) ◽  
pp. 2878-2887 ◽  
Author(s):  
Carol J. Mottram ◽  
Evangelos A. Christou ◽  
François G. Meyer ◽  
Roger M. Enoka

The rate of change in the fluctuations in motor output differs during the performance of fatiguing contractions that involve different types of loads. The purpose of this study was to examine the contribution of frequency modulation of motor unit discharge to the fluctuations in the motor output during sustained contractions with the force and position tasks. In separate tests with the upper arm vertical and the elbow flexed to 1.57 rad, the seated subjects maintained either a constant upward force at the wrist (force task) or a constant elbow angle (position task). The force and position tasks were performed in random order at a target force equal to 3.6 ± 2.1% (mean ± SD) of the maximal voluntary contraction (MVC) force above the recruitment threshold of an isolated motor unit from the biceps brachii. Each subject maintained the two tasks for an identical duration (161 ± 93 s) at a mean target force of 22.4 ± 13.6% MVC. As expected, the rate of increase in the fluctuations in motor output (force task: SD for detrended force; position task: SD for vertical acceleration) was greater for the position task than the force task ( P < 0.001). The amplitude of the coefficient of variation (CV) and the power spectra for motor unit discharge were similar between tasks ( P > 0.1) and did not change with time ( P > 0.1), and could not explain the different rates of increase in motor output fluctuations for the two tasks. Nonetheless, frequency modulation of motor unit discharge differed during the two tasks and predicted ( P < 0.001) both the CV for discharge rate (force task: 1–3, 12–13, and 14–15 Hz; position task: 0–1, and 1–2 Hz) and the fluctuations in motor output (force task: 5–6, 9–10, 12–13, and 14–15 Hz; position task: 6–7, 14–15, 17–19, 20–21, and 23–24 Hz). Frequency modulation of motor unit discharge rate differed for the force and position tasks and influenced the ability to sustain steady contractions.


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