Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise

G. A. Spirou, E. D. Young

Research output: Contribution to journalArticle

Abstract

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. 5. Responses of type IV units to notch noise, which is band-reject filtered noise with the center of the stop band placed at BF, were recorded. Plots of discharge rate versus notch width were constructed with the use of these data. These plots show excitatory responses to noise with narrow notches (less than a few kilohertz for units with BFs > 10 kHz) and inhibitory responses to noise with wider notches. 6. Units' response maps are used to generate predicted responses to notch noise signals, with the result that the responses of DCN neurons to the notch noise cannot be explained by a model in which stimulus energy in different frequency bands is weighted according to the response map and summed to produce the unit's output (quasilinear energy summation). The model predictions for narrow notches are usually the inverse of the actual responses of the units. However, the notch noise responses are consistent with response map features to the limited extent that there is a general correspondence between the width of the BFER a few decibels above threshold and the notch width at which the excitatory responses disappear. The notch noise data point up the fundamental nonlinearity of energy summation in DCN units and demonstrate the need for more sophisticated analysis of input-output relationships in this structure. These results can be explained, at least qualitatively, in terms of preliminary results on the organization of response maps in type II units.

Original languageEnglish (US)
Pages (from-to)1750-1768
Number of pages19
JournalJournal of Neurophysiology
Volume66
Issue number5
StatePublished - 1991

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Cochlear Nucleus
Noise
Pyramidal Cells
Neurons
Giant Cells
Electrodes
Cats

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise. / Spirou, G. A.; Young, E. D.

In: Journal of Neurophysiology, Vol. 66, No. 5, 1991, p. 1750-1768.

Research output: Contribution to journalArticle

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abstract = "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. 5. Responses of type IV units to notch noise, which is band-reject filtered noise with the center of the stop band placed at BF, were recorded. Plots of discharge rate versus notch width were constructed with the use of these data. These plots show excitatory responses to noise with narrow notches (less than a few kilohertz for units with BFs > 10 kHz) and inhibitory responses to noise with wider notches. 6. Units' response maps are used to generate predicted responses to notch noise signals, with the result that the responses of DCN neurons to the notch noise cannot be explained by a model in which stimulus energy in different frequency bands is weighted according to the response map and summed to produce the unit's output (quasilinear energy summation). The model predictions for narrow notches are usually the inverse of the actual responses of the units. However, the notch noise responses are consistent with response map features to the limited extent that there is a general correspondence between the width of the BFER a few decibels above threshold and the notch width at which the excitatory responses disappear. The notch noise data point up the fundamental nonlinearity of energy summation in DCN units and demonstrate the need for more sophisticated analysis of input-output relationships in this structure. These results can be explained, at least qualitatively, in terms of preliminary results on the organization of response maps in type II units.",
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N2 - 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. 5. Responses of type IV units to notch noise, which is band-reject filtered noise with the center of the stop band placed at BF, were recorded. Plots of discharge rate versus notch width were constructed with the use of these data. These plots show excitatory responses to noise with narrow notches (less than a few kilohertz for units with BFs > 10 kHz) and inhibitory responses to noise with wider notches. 6. Units' response maps are used to generate predicted responses to notch noise signals, with the result that the responses of DCN neurons to the notch noise cannot be explained by a model in which stimulus energy in different frequency bands is weighted according to the response map and summed to produce the unit's output (quasilinear energy summation). The model predictions for narrow notches are usually the inverse of the actual responses of the units. However, the notch noise responses are consistent with response map features to the limited extent that there is a general correspondence between the width of the BFER a few decibels above threshold and the notch width at which the excitatory responses disappear. The notch noise data point up the fundamental nonlinearity of energy summation in DCN units and demonstrate the need for more sophisticated analysis of input-output relationships in this structure. These results can be explained, at least qualitatively, in terms of preliminary results on the organization of response maps in type II units.

AB - 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. 5. Responses of type IV units to notch noise, which is band-reject filtered noise with the center of the stop band placed at BF, were recorded. Plots of discharge rate versus notch width were constructed with the use of these data. These plots show excitatory responses to noise with narrow notches (less than a few kilohertz for units with BFs > 10 kHz) and inhibitory responses to noise with wider notches. 6. Units' response maps are used to generate predicted responses to notch noise signals, with the result that the responses of DCN neurons to the notch noise cannot be explained by a model in which stimulus energy in different frequency bands is weighted according to the response map and summed to produce the unit's output (quasilinear energy summation). The model predictions for narrow notches are usually the inverse of the actual responses of the units. However, the notch noise responses are consistent with response map features to the limited extent that there is a general correspondence between the width of the BFER a few decibels above threshold and the notch width at which the excitatory responses disappear. The notch noise data point up the fundamental nonlinearity of energy summation in DCN units and demonstrate the need for more sophisticated analysis of input-output relationships in this structure. These results can be explained, at least qualitatively, in terms of preliminary results on the organization of response maps in type II units.

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