Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli

1994 ◽  
Vol 71 (6) ◽  
pp. 2446-2462 ◽  
Author(s):  
I. Nelken ◽  
E. D. Young

1. The principal cells of the dorsal cochlear nucleus (DCN) are mostly inhibited by best frequency (BF) tones but are mostly excited by broadband noise (BBN), producing the so-called type IV response characteristic. The narrowband inhibitory responses can be explained by the inhibitory influence of interneurons with type II response characteristics. However, it is not clear that all the details of the type IV responses can be accounted for by this neural circuit. In particular, many type IV units are inhibited by band-reject noise (notch noise); type II units tend to be only weakly excited by these stimuli, if at all. In this paper we study the relationships between the narrowband, inhibitory and the wideband, excitatory regimens of the type IV responses and present the case for the existence of a second inhibitory source in DCN, called the wideband inhibitor (WBI) below. 2. Type IV units were studied using pure tones, noise bands arithmetically centered on BF, notch noise centered on BF, and BBN. We measured the rate-level function (response rate as function of stimulus level) for each stimulus. This paper is based on the responses of 28 type IV units. 3. Evidence for low-threshold inhibitory input to type IV units is derived from analysis of rate-level functions at sound levels just above threshold. Notch noise stimuli of the appropriate notch width produce inhibition at threshold in this regime. When BBN is presented, this inhibition appears to summate with excitation produced by energy in the band of noise centered on BF, resulting in BBN rate-level functions with decreased slope and maximum firing rate. A range of slopes and maximal firing rates is observed, but these variables are strongly correlated and they are negatively correlated with the strength of the inhibition produced by notch noise; this result supports the conclusion that a single inhibitory source is responsible for these effects. 4. By contrast, there is a weak (nonsignificant) positive correlation between the strength of the inhibitory effect of notch noise and the slope/maximal firing rate in response to narrowband stimuli, including BF tones. The contrast between this positive nonsignificant correlation and the significant negative correlation mentioned above suggests that more than one inhibitory effect operates: specifically, the type II input is responsible for inhibition by narrowband stimuli and a different inhibitory source, the WBI, produces inhibition by notch stimuli. 5. Several lines of evidence are given to show that type II units cannot produce the inhibition seen with notch noise stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

1997 ◽  
Vol 78 (1) ◽  
pp. 229-247 ◽  
Author(s):  
Kevin A. Davis ◽  
Herbert F. Voigt

Davis, Kevin A. and Herbert F. Voigt. Evidence of stimulus-dependent correlated activity in the dorsal cochlear nucleus of decerebrate gerbils. J. Neurophysiol. 78: 229–247, 1997. Cross-correlation analysis of simultaneously recorded spike trains was used to study the internal organization of the dorsal cochlear nucleus (DCN) of unanesthetized decerebrate Mongolian gerbils. The goal was to test the model (adapted from cat) that its principal cells (type III and type IV units) receive three sources of shared auditory input: excitatory input from the auditory nerve; inhibitory input from DCN interneurons (vertical cells; type II and typeIII-i units) that respond vigorously to tones; and inhibitory input from ventral cochlear nucleus principal cells (D-stellate cells; wideband inhibitors) that conversely respond vigorously to noise. Records of spontaneous and/or driven activities (to long-duration tones and frozen broadband noise) were obtained for 51 pairs consisting of type II, type III, and type IV units; type III units inhibited by low-level noise were subclassified as type III-i units. Pairs were isolated with two electrodes to study the effect of differences in unit best frequencies (BFs) on correlation. All correlated pairs composed of type III and type IV units (17 of 31 pairs) showed central mounds (CMs), indicative of shared input, in their cross-correlograms. These data exhibited two important properties: pairs with similar BFs were more likely to show CMs, and the shape of the CMs was stimulus dependent. That is, CM width typically changed sharply from wide to narrow with increasing level; significantly, transition-level CMs were either a composite of these shapes or not present. The transition to only narrow CMs occurred above the thresholds of type II and type III-i units to tones, but below their thresholds to noise. Cross-correlograms derived from the tone-evoked activities of pairs involving type II units (3 of 6 pairs) showed inhibitory troughs (ITs); unexpectedly, type III-i units were involved in both IT and CM pairs, suggesting that this unit type may reflect recordings from both vertical and principal cells. Overall, the results are interpretable in terms of the model of gerbil DCN that was adapted from cat, suggesting that the model generalizes across species. Compared with cat, however, gerbil principal cell responses (predominantly type III unit properties) are less dominated by inhibition.


1997 ◽  
Vol 78 (2) ◽  
pp. 790-799 ◽  
Author(s):  
Israel Nelken ◽  
Eric D. Young

Nelken, Israel and Eric D. Young. Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. I. Regions of linear interaction. J. Neurophysiol. 78: 790–799, 1997. The principal neurons of the dorsal cochlear nucleus have complex response properties, many of which are classified as type IV. These units integrate energy in the acoustic signal in a nonlinear fashion; for example, at high sound levels the response to a noise of narrow bandwidth and to a band-reject filtered noise with a spectral notch of the same bandwidth may both be inhibitory. However, the sum of these two stimuli, which is broadband noise (BBN), generally gives an excitatory response. In other situations, linear interactions among stimulus components are observed. In this paper, three regimes of approximate linearity were identified. First, best-frequency (BF) tones and equal-energy narrow noisebands centered at BF evoke almost the same response, which is consistent with a stage of linear filtering followed by a nonlinearity that generates the rate responses of the neuron. Second, for sounds close to threshold (10–15 dB re threshold), energy over the full bandwidth of the unit is integrated linearly. Within this regime, responses to the narrow noiseband and the spectral notch mentioned above do sum to equal the response to BBN. Finally, two noisebands centered at different frequencies, such that their sum is a notch in a broad band of noise, sum linearly at low sound levels; the degree of linearity improves as the separation between the noisebands increases. The results are interpreted in terms of a model of type IV response generation containing two inhibitory interneurons: type II units, which are active for narrowband stimuli, including tones, and the wideband inhibitor, which is active for broadband stimuli. In most cases, the onset of nonlinearity occurs for stimuli that significantly activate the type II inhibitory interneuron.


1999 ◽  
Vol 82 (2) ◽  
pp. 1019-1032 ◽  
Author(s):  
William S. Rhode

The dorsal cochlear nucleus receives input from the auditory nerve and relays acoustic information to the inferior colliculus. Its principal cells receive two systems of inputs. One system through the molecular layer carries multimodal information that is processed through a neuronal circuit that resembles the cerebellum. A second system through the deep layer carries primary auditory nerve input, some of which is relayed through interneurons. The present study reveals the morphology of individual interneurons and their local axonal arbors and how these inhibitory interneurons respond to sound. Vertical cells lie beneath the fusiform cell layer. Their dendritic and axonal arbors are limited to an isofrequency lamina. They give rise to pericellular nests around the base of fusiform cells and their proximal basal dendrites. These cells exhibit an onset-graded response to short tones and have response features defined as type II. They have tuning curves that are closed contours (0 shaped), thresholds ∼27 dB SPL, spontaneous firing rates of ∼0 spikes/s, and they respond weakly or not at all to broadband noise, as described for type II units. Their responses are nonmonotonic functions of intensity with peak responses between 30 and 60 dB SPL. They also show a preference for the high-to-low direction of a frequency sweep. It has been suggested that these circuits may be involved in the processing of spectral cues for the localization of sound sources.


1976 ◽  
Vol 39 (2) ◽  
pp. 282-300 ◽  
Author(s):  
E. D. Young ◽  
W. E. Brownell

1. Single-unit responses in the dorsal cochlear nucleus of unanesthetized, decerebrate cats have been divided into two categoreis. These have been differentiated on the basis of responses to best-frequency tones. Type IV units responded to best-frequency tones with excitation from threshold to about 20 or 30 dB above threshold; at higher levels, their response was inhibitory. In a few cases, the excitatory area near threshold was not seen and in a few others, the response became excitatory again at high levels. Type IV units could be divided into two groups based on the length of time that inhibition was maintained in response to long tones. Type IV units are not seen in anesthetized cats. 2. Type II/III units responded to best-frequency tones of all levels with excitation. Nonmonotonic rate versus level functions were seen in type II/III units, but they were of much less drastic character; the discharge rate of nonmonotonic type II/III units was still well above spontaneous rate for tones 50 dB above threshold. Type II/III units defined in this way were found to have, on the average, lower rates of spontaneous activity and higher thresholds than type IV units. 3. Type II/III units responded weakly to broad-band noise in comparison to auditory nerve fibers and many of them did not respond at all to noise. Type IV units, with best frequencies above 0.9 kHz, gave excitatory responses to noise. 4. The inhibitory response areas of type IV units could be divided into two areas: a central inhibitory area in the vicinity of best frequency where on- and off-discharges and afterdischarges were seen; and inhibitory side bands at higher and lower frequencies where simple inhibitory responses were seen. In four units, it was possible to show that the central inhibitory area was converted to an excitatory area after administration of an anesthetic dose of pentobarbital. 5. Most type II/III and type IV units could be excited or inhibited by stimuli in the contralateral ear. Broad-band noise was a more effective contralateral stimulus than tones at the ipsilateral best frequency. 6. On the basis of the properties of type II/III and type IV cells, it is suggested that type II/III responses are recorded from interneurons which provide a large share of the inhibitory imput to type IV cells.


1999 ◽  
Vol 82 (2) ◽  
pp. 648-663 ◽  
Author(s):  
George A. Spirou ◽  
Kevin A. Davis ◽  
Israel Nelken ◽  
Eric D. Young

The type II unit is a prominent inhibitory interneuron in the dorsal cochlear nucleus (DCN), most likely recorded from vertical cells. Type II units are characterized by low rates of spontaneous activity, weak responses to broadband noise, and vigorous, narrowly tuned responses to tones. The weak responses of type II units to broadband stimuli are unusual for neurons in the lower auditory system and suggest that these units receive strong inhibitory inputs, most likely from onset-C neurons of the ventral cochlear nucleus. The question of the definition of type II units is considered here; the characteristics listed in the preceding text define a homogeneous type II group, but the boundary between this group and other low spontaneous rate neurons in DCN (type I/III units) is not yet clear. Type II units in decerebrate cats were studied using a two-tone paradigm to map inhibitory responses to tones and using noisebands of varying width to study the inhibitory processes evoked by broadband stimuli. Iontophoresis of bicuculline and strychnine and comparisons of two-tone responses between type II units and auditory nerve fibers were used to differentiate inhibitory processes occurring near the cell from two-tone suppression in the cochlea. For type II units, a significant inhibitory region is always seen with two-tone stimuli; the bandwidth of this region corresponds roughly to the previously reported excitatory bandwidth of onset-C neurons. Bandwidth widening experiments with noisebands show a monotonic decline in response as the bandwidth increases; these data are interpreted as revealing strong inhibitory inputs with properties more like onset-C neurons than any other response type in the lower auditory system. Consistent with these properties, iontophoresis of inhibitory antagonists produces a large increase in discharge rate to broadband noise, making tone and noise responses nearly equal.


1997 ◽  
Vol 78 (2) ◽  
pp. 800-811 ◽  
Author(s):  
Israel Nelken ◽  
Peter J. Kim ◽  
Eric D. Young

Nelken, Israel, Peter J. Kim, and Eric D. Young. Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. II. Predicting responses with the use of nonlinear models. J. Neurophysiol. 78: 800–811, 1997. Two nonlinear modeling methods were used to characterize the input/output relationships of type IV units, which are one principal cell type in the dorsal cochlear nucleus (DCN). In both cases, the goal was to derive predictive models, i.e., models that could predict the responses to other stimuli. In one method, frequency integration was estimated from response maps derived from single tones and simultaneous pairs of tones presented over a range of frequencies. This model combined linear integration of energy across frequency and nonlinear interactions of energy at different frequencies. The model was used to predict responses to noisebands with varying width and center frequency. In almost all cases, predictions using two-tone interactions were better than linear predictions based on single-tone responses only. In about half the cases, reasonable quantitative fits were achieved. The fits were best for noisebands with narrow bandwidth and low sound levels. In the second nonlinear method, the spectrotemporal receptive field (STRF) was derived from responses to broadband stimuli. The STRF could account for some qualitative features of the responses to broad noisebands and spectral notches embedded in broad noisebands. Quantitatively, however, the STRFs failed to predict the responses of type IV units even to simple broadband noise stimuli. For narrowband stimuli, the STRF failed to predict even qualitative features (such as excitatory and inhibitory frequency bands). The responses of DCN type IV units presumably result from interactions of two inhibitory sources, a strong one that is preferentially activated by narrowband stimuli and a weaker one that is preferentially activated by broadband stimuli. The results presented here suggest that the STRF measures effects related to the broadband inhibition, whereas two-tone interactions measure mostly effects related to narrowband inhibition. This explains why models based on two-tone interactions predict the responses to narrow noisebands much better then models based on STRFs. It is concluded that a minimal stimulus set for characterizing type IV units must contain both broadband and narrowband stimuli, because each stimulus class by itself activates only partially the integration mechanisms that shape the responses of type IV units. Similar conclusions are expected to hold in other parts of the auditory system: when characterizing a complex auditory unit, it is necessary to use a range of stimuli to ensure that all integration mechanisms are activated.


1990 ◽  
Vol 64 (5) ◽  
pp. 1590-1610 ◽  
Author(s):  
H. F. Voigt ◽  
E. D. Young

1. Cross-correlation analysis was used to study the organization of inhibitory connections between type II or type III units and type IV principal cells in cat dorsal cochlear nucleus (DCN). Pairs of units were isolated using two microelectrodes so that information about the distance over which connections are made could be analyzed. Data were obtained from 51 pairs consisting of a type II and a type IV unit and from 22 pairs consisting of a type III and a type IV unit. The analyses in this paper concentrate on type II-type IV pairs. 2. Inhibitory troughs (ITs) are observed in the cross-correlograms of type II-type IV pairs (21/51 cases). An IT is a transient decrease in discharge probability in the postsynaptic (type IV) unit immediately after spikes in the presynaptic unit (type II). The average latency to the start of ITs is 0.73 ms, and the troughs are asymmetric with a faster leading phase. Small excitatory peaks accompany the ITs in type II units, but these are probably secondary effects associated with the IT. ITs are consistent with a monosynaptic, inhibitory connection between type II and type IV units. A variety of evidence suggests that type II responses are recorded from vertical cells, an interneuron in the deep layer of the DCN that may be glycinergic. 3. The cross-correlograms of type III-type IV pairs are more complex and variable than those of type II-type IV pairs--ITs are seen in 4/22 cases, and peaks of correlation that are symmetrically located around the origin (central mound or CM) are seen in 4/22 cases; two cases have both an IT and a CM. CMs result from shared sources of input. Whereas type II-type IV correlogram features change primarily in amplitude as stimulus conditions change, correlogram features in some type III-type IV pairs change qualitatively with stimulus conditions; correlograms are flat for some stimuli and show ITs or CMs or mixtures of the two for others. This variability suggests that the circuitry associated with type III-type IV pairs is more complex than a monosynaptic connection, and further analysis of type III-type IV pairs was not done. 4. The strength of inhibition for an IT is measured as the area under the IT (effectiveness) and as effectiveness divided by the postsynaptic discharge rate (association index).(ABSTRACT TRUNCATED AT 400 WORDS)


1991 ◽  
Vol 66 (5) ◽  
pp. 1750-1768 ◽  
Author(s):  
G. A. Spirou ◽  
E. D. Young

1. Response maps of 49 type IV neurons in cat dorsal cochlear nucleus (DCN) were studied by moving a tone in small steps along the frequency dimension and along the intensity dimension. Type IV responses are recorded from DCN principal cells. Data were collected from 38 units with best frequencies (BFs) from 2.16 to 50.3 kHz with the use of electrode penetrations along the long (strial) axis of the DCN; an additional 11 units from a previous study were analyzed. A stereotypical type IV response map is defined as consisting of two excitatory and two inhibitory regions. Type IV units from both the pyramidal cell layer (probably pyramidal cells) and the deep layer (probably giant cells) show the same types of response maps. 2. Two of the regions, one excitatory and one inhibitory, are seen in all type IV units. These regions are a low-threshold excitatory region at best frequency (BFER) and an inhibitory area at higher levels, usually centered below BF but extending upward in frequency to include BF (central inhibitory area, or CIA). The high resolution of the response maps in this paper allows us to show that type IV units fall into two groups on the basis of whether their CIAs are narrow with well-defined borders (35 units) or broad with poorly defined borders (14 units). 3. Two additional features of type IV response maps can be defined, most consistently in units with well-defined CIAs. These features are an excitatory region along the high-frequency edge of the CIA (upper excitatory region, UER) and an upper inhibitory sideband (UIS). The BFER and UER are continuous in many units, but in some cases their continuity is broken by the CIA. It seems likely that the BFER and UER represent a single excitatory input to type IV units and are revealed because the tuning curve of the stronger inhibitory inputs that produce the CIA has thresholds greater than and BFs lower than the excitatory inputs. 4. The CIA is probably produced by inhibitory inputs from DCN type II neurons. The bandwidths of type IV CIAs are about 1–3 times larger (at 40 dB above threshold) than the excitatory bandwidths of DCN type II units, suggesting a convergence of the equivalent in tuning of about two type II units onto each type IV unit. The BF of the CIA is below the excitatory BF of the type IV unit in most cases.(ABSTRACT TRUNCATED AT 400 WORDS)


1996 ◽  
Vol 76 (3) ◽  
pp. 1667-1688 ◽  
Author(s):  
S. E. Stabler ◽  
A. R. Palmer ◽  
I. M. Winter

1. We examined the temporal and mean rate discharge characteristics of 514 single units recorded extracellularly from the dorsal cochlear nucleus (DCN) of anesthetized guinea pigs. A mean rate response area (receptive field) was measured for the majority of units in this study. Each response area was placed in one of seven categories (type I to type V and the intermediate types I/III and IV-T) as defined by previous workers. The shape of the best frequency (BF) rate-level function has been used to aid in the distinction between type IV and type IV-T units, and the classification of type II units is based on their relative response to noise and tone bursts. 2. The threshold of single units was normalized to the cochlear action potential (CAP) threshold (a negative relative threshold indicates that the unit's threshold was more sensitive than the corresponding CAP threshold). There were significant differences (P < 0.05; 1-way analysis of variance--Duncan test) between the mean relative thresholds of type IV units (-12 dB) and those of type I (-6.52 dB), type II (-3 dB), and type I/III units (-4.25 dB). There were also significant differences between the relative thresholds of types III and IV-T and those of types I/III and II. 3. Rate-level functions at a unit's BF were divided into groups according to shape and degree of nonmonotonicity. Six units responded with a decrease in firing rate at all suprathreshold sound levels. However, most units increased their discharge rate over approximately the first 20 dB above BF threshold. Units were further subdivided by the change in slope 20 dB above BF threshold. The majority of units (60%) showed monotonic increases in discharge rate with sound level: some rate-level functions clearly resembled the sloping saturation rate-level functions observed in intermediate-threshold auditory nerve fibers. An unexpected finding was the relatively large number of nonmonotonic rate-level functions (40%). Among a relatively homogenous group of projection neurons (predominantly type IV and pause/build units) with nonmonotonic rate-level functions, the range of "best intensities" (the sound level evoking the highest discharge rate) was < 50 dB. This range of best intensities is narrower than found in higher auditory nuclei. 4. Units were also classified by their temporal activity pattern in response to suprathreshold BF tones. The most common pattern identified is the pause/build pattern (n = 294). This temporal activity pattern has been associated with the principal output neuron of the DCN, the fusiform cell. Our definition of pause/build units includes units with an almost constant steady-state discharge rate. Nonmonotonic rate-level functions were observed in 42% (99 of 233) of pause/build units. A measure of discharge regularity (the SD of the interspike interval/mean interspike interval: coefficient of variation, CV) revealed that the majority (82%) of units classified as pause/build and with steady-state discharge rates > 75 spikes/s (n = 142) were characterized by regular discharge patterns (CV = 0.41 +/- 0.15, mean +/- SD). 5. Units characterized by chopper or onset-type discharges were the next most frequently encountered units. The chopper units (n = 75) showed a regular discharge (CV = 0.39 +/- 0.17) similar to that found in recordings from the ventral division of the cochlear nucleus (VCN). One difference between many chopper units in the DCN compared with those recorded in the VCN was the relatively high value (> 5 ms) of the mean interspike interval (and thus the low steady-state discharge rate). The majority (44 of 59; 75%) of chopper units had monotonic rate-level functions. Onset units (n = 47) may represent several response types, linked by the predominance of discharges in response to stimulus onset, and the majority of onset units reported here bear little resemblance to onset units recorded in the VCN of the guinea pig. Approximately 10% of units did not fit easily into any of th


1988 ◽  
Vol 59 (3) ◽  
pp. 1014-1032 ◽  
Author(s):  
H. F. Voigt ◽  
E. D. Young

1. Cross-correlation analysis of simultaneously recorded spike trains can be used to gain insight into functional interactions among neurons. In this paper, we report on cross-correlation analysis of neuron pairs in the dorsal cochlear nucleus (DCN) of the cat. Neuron pairs were isolated with two independent electrodes, which allow systematic study of the effects on correlation of distances between units and differences in their best frequencies (BFs). The data in this paper were obtained from 51 pairs consisting of two neurons of the same type. 2. Cross-correlograms were obtained for 35 pairs composed of type IV units, which are recorded from the principal cells of the DCN. Pairs of type IV units with correlated activities give cross-correlograms with increased correlation near zero delay. This feature is called a central mound (CM) and most likely results from shared excitatory or shared inhibitory inputs. 3. Records of spontaneous activity were obtained from 31 pairs of type IV units. Six of these pairs have correlated spontaneous activities. All six pairs have BFs that differ by less than 0.2 octaves. The shared input inducing these correlations must be a spontaneously active and tonotopically organized projection, like the auditory nerve. Type II units, thought to be DCN inhibitory interneurons that project to type IV units, are not spontaneously active, and thus cannot be the cause of correlated spontaneous activity. Similarly, cochlear granule cells, whose axons project orthogonally to the tonotopic sheets of DCN, cannot be the cause of correlated spontaneous activity because their projection is not confined tonotopically. 4. Stimulus-driven activities were studied for 12 type IV pairs that have uncorrelated spontaneous activities. Five of these pairs have correlated driven activities, with CMs whose sizes depend on the frequency and sound level of the acoustic stimulus. A frequency vs. sound level correlation response map shows the V-shaped tuning properties of the correlation-inducing mechanism. The properties of stimulus-driven correlation in these type IV pairs are consistent with the hypothesis that the correlation is induced by shared input from DCN type II units, although this is not the only possibility. 5. All six type IV pairs with correlated spontaneous activities have correlated driven activities. In five of these pairs, the degree of correlation decreases from its value with spontaneous activity when a low-level acoustic stimulus is applied. Three of these five pairs were tested at higher stimulus levels.(ABSTRACT TRUNCATED AT 400 WORDS)


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