Binaural processing of sound pressure level in cat primary auditory cortex: Evidence for a representation based on absolute levels rather than interaural level differences

Malcolm Semple, L. M. Kitzes

Research output: Contribution to journalArticle

Abstract

1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (>90%) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in >60% of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to ABL; at other values of ILD the relation was often monotonic. For many units, response strength was nonmonotonically related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2% of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear. Accordingly, the binaural sensitivity previously described in terms of ILD and ABL is sufficiently described in terms of binaural SPL: the typical auditory cortical neuron has a clearly defined focus of maximum excitatory response strength that is associated with a limited range of SPL at each ear. The optimal range of SPLs is usually different for each ear. There is typically a systematic reduction in response strength with any systematic departure from the best binaural combination of SPLs. Thus the results reported here provide evidence that auditory cortical responses are more aptly interpreted in terms of the absolute levels at each ear, rather than by a relative, derivative index, such as ILD or ABL.

Original languageEnglish (US)
Pages (from-to)449-461
Number of pages13
JournalJournal of Neurophysiology
Volume69
Issue number2
StatePublished - 1993

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Auditory Cortex
Cats
Neurons
Pressure
Ear
Inferior Colliculi
Cues
Gerbillinae

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

@article{7c1a1982b3ff439dbc85b6a91d3e0df1,
title = "Binaural processing of sound pressure level in cat primary auditory cortex: Evidence for a representation based on absolute levels rather than interaural level differences",
abstract = "1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (>90{\%}) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in >60{\%} of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to ABL; at other values of ILD the relation was often monotonic. For many units, response strength was nonmonotonically related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2{\%} of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear. Accordingly, the binaural sensitivity previously described in terms of ILD and ABL is sufficiently described in terms of binaural SPL: the typical auditory cortical neuron has a clearly defined focus of maximum excitatory response strength that is associated with a limited range of SPL at each ear. The optimal range of SPLs is usually different for each ear. There is typically a systematic reduction in response strength with any systematic departure from the best binaural combination of SPLs. Thus the results reported here provide evidence that auditory cortical responses are more aptly interpreted in terms of the absolute levels at each ear, rather than by a relative, derivative index, such as ILD or ABL.",
author = "Malcolm Semple and Kitzes, {L. M.}",
year = "1993",
language = "English (US)",
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pages = "449--461",
journal = "Journal of Neurophysiology",
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publisher = "American Physiological Society",
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T1 - Binaural processing of sound pressure level in cat primary auditory cortex

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AU - Semple, Malcolm

AU - Kitzes, L. M.

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N2 - 1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (>90%) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in >60% of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to ABL; at other values of ILD the relation was often monotonic. For many units, response strength was nonmonotonically related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2% of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear. Accordingly, the binaural sensitivity previously described in terms of ILD and ABL is sufficiently described in terms of binaural SPL: the typical auditory cortical neuron has a clearly defined focus of maximum excitatory response strength that is associated with a limited range of SPL at each ear. The optimal range of SPLs is usually different for each ear. There is typically a systematic reduction in response strength with any systematic departure from the best binaural combination of SPLs. Thus the results reported here provide evidence that auditory cortical responses are more aptly interpreted in terms of the absolute levels at each ear, rather than by a relative, derivative index, such as ILD or ABL.

AB - 1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (>90%) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in >60% of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to ABL; at other values of ILD the relation was often monotonic. For many units, response strength was nonmonotonically related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2% of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear. Accordingly, the binaural sensitivity previously described in terms of ILD and ABL is sufficiently described in terms of binaural SPL: the typical auditory cortical neuron has a clearly defined focus of maximum excitatory response strength that is associated with a limited range of SPL at each ear. The optimal range of SPLs is usually different for each ear. There is typically a systematic reduction in response strength with any systematic departure from the best binaural combination of SPLs. Thus the results reported here provide evidence that auditory cortical responses are more aptly interpreted in terms of the absolute levels at each ear, rather than by a relative, derivative index, such as ILD or ABL.

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