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Sparse representation of sounds in the unanesthetized auditory cortex.

Hromádka T, Deweese MR, Zador AM - PLoS Biol. (2008)

Bottom Line: Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported.Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex.Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Watson School of Biological Sciences, Cold Spring Harbor, New York, United States of America.

ABSTRACT
How do neuronal populations in the auditory cortex represent acoustic stimuli? Although sound-evoked neural responses in the anesthetized auditory cortex are mainly transient, recent experiments in the unanesthetized preparation have emphasized subpopulations with other response properties. To quantify the relative contributions of these different subpopulations in the awake preparation, we have estimated the representation of sounds across the neuronal population using a representative ensemble of stimuli. We used cell-attached recording with a glass electrode, a method for which single-unit isolation does not depend on neuronal activity, to quantify the fraction of neurons engaged by acoustic stimuli (tones, frequency modulated sweeps, white-noise bursts, and natural stimuli) in the primary auditory cortex of awake head-fixed rats. We find that the population response is sparse, with stimuli typically eliciting high firing rates (>20 spikes/second) in less than 5% of neurons at any instant. Some neurons had very low spontaneous firing rates (<0.01 spikes/second). At the other extreme, some neurons had driven rates in excess of 50 spikes/second. Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported. Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex. Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.

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Only a Small Fraction of the Population Showed a Well-Driven Stimulus-Evoked Response at Any Instant(A) Cumulative fraction of stimulus-evoked changes in firing rate for various stimuli. Different colors correspond to different stimuli: black: 30 or 40 dB tones (n = 91 neurons, 1,365 response bins); blue: 50 or 60 dB tones (n =145 neurons, 2,079 response bins); red: 80 dB tones (n = 22 neurons, 330 bins); orange: FM sweeps (n = 22 neurons, 704 bins); purple: 80 dB white-noise bursts (n = 23 neurons, 69 bins); and green: natural sounds (n = 27 neurons, 18,900 bins).(B) Fractions of response bins showing well driven (>20 sp/s) stimulus-evoked change in firing rate were low for all stimulus ensembles used. Error bars show standard error determined by bootstrapping.
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pbio-0060016-g005: Only a Small Fraction of the Population Showed a Well-Driven Stimulus-Evoked Response at Any Instant(A) Cumulative fraction of stimulus-evoked changes in firing rate for various stimuli. Different colors correspond to different stimuli: black: 30 or 40 dB tones (n = 91 neurons, 1,365 response bins); blue: 50 or 60 dB tones (n =145 neurons, 2,079 response bins); red: 80 dB tones (n = 22 neurons, 330 bins); orange: FM sweeps (n = 22 neurons, 704 bins); purple: 80 dB white-noise bursts (n = 23 neurons, 69 bins); and green: natural sounds (n = 27 neurons, 18,900 bins).(B) Fractions of response bins showing well driven (>20 sp/s) stimulus-evoked change in firing rate were low for all stimulus ensembles used. Error bars show standard error determined by bootstrapping.

Mentions: What is the typical response across the entire neuronal population to a particular stimulus? Figure 5 shows the cumulative distribution of firing rate changes (with respect to baseline) for each of the stimuli tested. To simplify the interpretation of these cumulative distributions, we defined an arbitrary threshold of 20 sp/s, beyond which we labeled the response as “well-driven;” Figure 5B shows the fraction of neuronal population exceeding this threshold for each ensemble. The choice of 20 sp/s, which corresponds to only a single extra spike in the 50-ms response bin, we consider was quite conservative; for example, other authors have chosen a higher (arbitrary) value of 50 sp/s as the threshold for the “high-firing” regime [27].


Sparse representation of sounds in the unanesthetized auditory cortex.

Hromádka T, Deweese MR, Zador AM - PLoS Biol. (2008)

Only a Small Fraction of the Population Showed a Well-Driven Stimulus-Evoked Response at Any Instant(A) Cumulative fraction of stimulus-evoked changes in firing rate for various stimuli. Different colors correspond to different stimuli: black: 30 or 40 dB tones (n = 91 neurons, 1,365 response bins); blue: 50 or 60 dB tones (n =145 neurons, 2,079 response bins); red: 80 dB tones (n = 22 neurons, 330 bins); orange: FM sweeps (n = 22 neurons, 704 bins); purple: 80 dB white-noise bursts (n = 23 neurons, 69 bins); and green: natural sounds (n = 27 neurons, 18,900 bins).(B) Fractions of response bins showing well driven (>20 sp/s) stimulus-evoked change in firing rate were low for all stimulus ensembles used. Error bars show standard error determined by bootstrapping.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2214813&req=5

pbio-0060016-g005: Only a Small Fraction of the Population Showed a Well-Driven Stimulus-Evoked Response at Any Instant(A) Cumulative fraction of stimulus-evoked changes in firing rate for various stimuli. Different colors correspond to different stimuli: black: 30 or 40 dB tones (n = 91 neurons, 1,365 response bins); blue: 50 or 60 dB tones (n =145 neurons, 2,079 response bins); red: 80 dB tones (n = 22 neurons, 330 bins); orange: FM sweeps (n = 22 neurons, 704 bins); purple: 80 dB white-noise bursts (n = 23 neurons, 69 bins); and green: natural sounds (n = 27 neurons, 18,900 bins).(B) Fractions of response bins showing well driven (>20 sp/s) stimulus-evoked change in firing rate were low for all stimulus ensembles used. Error bars show standard error determined by bootstrapping.
Mentions: What is the typical response across the entire neuronal population to a particular stimulus? Figure 5 shows the cumulative distribution of firing rate changes (with respect to baseline) for each of the stimuli tested. To simplify the interpretation of these cumulative distributions, we defined an arbitrary threshold of 20 sp/s, beyond which we labeled the response as “well-driven;” Figure 5B shows the fraction of neuronal population exceeding this threshold for each ensemble. The choice of 20 sp/s, which corresponds to only a single extra spike in the 50-ms response bin, we consider was quite conservative; for example, other authors have chosen a higher (arbitrary) value of 50 sp/s as the threshold for the “high-firing” regime [27].

Bottom Line: Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported.Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex.Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Watson School of Biological Sciences, Cold Spring Harbor, New York, United States of America.

ABSTRACT
How do neuronal populations in the auditory cortex represent acoustic stimuli? Although sound-evoked neural responses in the anesthetized auditory cortex are mainly transient, recent experiments in the unanesthetized preparation have emphasized subpopulations with other response properties. To quantify the relative contributions of these different subpopulations in the awake preparation, we have estimated the representation of sounds across the neuronal population using a representative ensemble of stimuli. We used cell-attached recording with a glass electrode, a method for which single-unit isolation does not depend on neuronal activity, to quantify the fraction of neurons engaged by acoustic stimuli (tones, frequency modulated sweeps, white-noise bursts, and natural stimuli) in the primary auditory cortex of awake head-fixed rats. We find that the population response is sparse, with stimuli typically eliciting high firing rates (>20 spikes/second) in less than 5% of neurons at any instant. Some neurons had very low spontaneous firing rates (<0.01 spikes/second). At the other extreme, some neurons had driven rates in excess of 50 spikes/second. Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported. Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex. Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.

Show MeSH