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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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The Distribution of Firing Rates Follows a Lognormal Distribution(A) Cells were characterized by their activity during each of the response epochs: spontaneous, early, late, and off, each 50 ms long. Spontaneous epochs cover spontaneous activity before the stimulus, early and late epochs cover first and second half of the stimulus duration (100 ms), respectively, and off epochs cover 50-ms period after stimulus termination. In frequency space, individual trials were grouped into one-octave-wide bins, and averaged to provide a firing rate value for each octave bin. This figure shows a spike raster plot for an example neuron (with a sustained excitatory response), where each row represents a single trial, and each dot marks the occurrence of a spike. Shown are responses to 1–40 kHz tones (60 dB SPL, left ordinate.) Individual trials were grouped into five spontaneous, and 15 evoked response bins (right ordinate.) Note that the top quarter of an octave is not included in any of the bins.(B and C) Firing rates of most neurons were low and followed a lognormal distribution.(B) Frequency histogram of nonzero spontaneous firing rates in individual octave bins (n = 567 octave bins, from 145 neurons). Each neuron contributed a maximum of four or five data points (because each neuron had four or five octave bins per epoch). The filled arrow shows the position of the median spontaneous firing rate, and the open arrow shows the position of the mean spontaneous firing rate.(C) The distribution of spontaneous firing rates (dots) was fit with a lognormal distribution (gray line), the mean and variance of which were given by the mean and variance of the original firing rate distribution (see Materials and Methods). The lognormal distribution appears as a normal distribution on a (semi-) logarithmic scale. The error bars show 95% confidence intervals determined by bootstrapping.
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pbio-0060016-g003: The Distribution of Firing Rates Follows a Lognormal Distribution(A) Cells were characterized by their activity during each of the response epochs: spontaneous, early, late, and off, each 50 ms long. Spontaneous epochs cover spontaneous activity before the stimulus, early and late epochs cover first and second half of the stimulus duration (100 ms), respectively, and off epochs cover 50-ms period after stimulus termination. In frequency space, individual trials were grouped into one-octave-wide bins, and averaged to provide a firing rate value for each octave bin. This figure shows a spike raster plot for an example neuron (with a sustained excitatory response), where each row represents a single trial, and each dot marks the occurrence of a spike. Shown are responses to 1–40 kHz tones (60 dB SPL, left ordinate.) Individual trials were grouped into five spontaneous, and 15 evoked response bins (right ordinate.) Note that the top quarter of an octave is not included in any of the bins.(B and C) Firing rates of most neurons were low and followed a lognormal distribution.(B) Frequency histogram of nonzero spontaneous firing rates in individual octave bins (n = 567 octave bins, from 145 neurons). Each neuron contributed a maximum of four or five data points (because each neuron had four or five octave bins per epoch). The filled arrow shows the position of the median spontaneous firing rate, and the open arrow shows the position of the mean spontaneous firing rate.(C) The distribution of spontaneous firing rates (dots) was fit with a lognormal distribution (gray line), the mean and variance of which were given by the mean and variance of the original firing rate distribution (see Materials and Methods). The lognormal distribution appears as a normal distribution on a (semi-) logarithmic scale. The error bars show 95% confidence intervals determined by bootstrapping.

Mentions: We first analyzed the basic population response elicited by tones, beginning with the response to tones presented at 50 or 60 decibels (dB SPL). We divided the tone-evoked response into four 50-millisecond (ms) long “epochs”: spontaneous, early, late, and off (Figure 3A, also see Materials and Methods). To ensure a sufficient number of trials for assessing the statistical significance of putative changes in firing rate over background, we grouped responses across nearby frequencies (one-octave-wide bins; four- or five-octave bins for each response epoch). Control analyses using narrower (half-octave) bins gave similar results (see Materials and Methods), as expected from the relatively broad frequency tuning of neurons in the rat primary auditory cortex [22,23]; see also [24].


Sparse representation of sounds in the unanesthetized auditory cortex.

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

The Distribution of Firing Rates Follows a Lognormal Distribution(A) Cells were characterized by their activity during each of the response epochs: spontaneous, early, late, and off, each 50 ms long. Spontaneous epochs cover spontaneous activity before the stimulus, early and late epochs cover first and second half of the stimulus duration (100 ms), respectively, and off epochs cover 50-ms period after stimulus termination. In frequency space, individual trials were grouped into one-octave-wide bins, and averaged to provide a firing rate value for each octave bin. This figure shows a spike raster plot for an example neuron (with a sustained excitatory response), where each row represents a single trial, and each dot marks the occurrence of a spike. Shown are responses to 1–40 kHz tones (60 dB SPL, left ordinate.) Individual trials were grouped into five spontaneous, and 15 evoked response bins (right ordinate.) Note that the top quarter of an octave is not included in any of the bins.(B and C) Firing rates of most neurons were low and followed a lognormal distribution.(B) Frequency histogram of nonzero spontaneous firing rates in individual octave bins (n = 567 octave bins, from 145 neurons). Each neuron contributed a maximum of four or five data points (because each neuron had four or five octave bins per epoch). The filled arrow shows the position of the median spontaneous firing rate, and the open arrow shows the position of the mean spontaneous firing rate.(C) The distribution of spontaneous firing rates (dots) was fit with a lognormal distribution (gray line), the mean and variance of which were given by the mean and variance of the original firing rate distribution (see Materials and Methods). The lognormal distribution appears as a normal distribution on a (semi-) logarithmic scale. The error bars show 95% confidence intervals determined by bootstrapping.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2214813&req=5

pbio-0060016-g003: The Distribution of Firing Rates Follows a Lognormal Distribution(A) Cells were characterized by their activity during each of the response epochs: spontaneous, early, late, and off, each 50 ms long. Spontaneous epochs cover spontaneous activity before the stimulus, early and late epochs cover first and second half of the stimulus duration (100 ms), respectively, and off epochs cover 50-ms period after stimulus termination. In frequency space, individual trials were grouped into one-octave-wide bins, and averaged to provide a firing rate value for each octave bin. This figure shows a spike raster plot for an example neuron (with a sustained excitatory response), where each row represents a single trial, and each dot marks the occurrence of a spike. Shown are responses to 1–40 kHz tones (60 dB SPL, left ordinate.) Individual trials were grouped into five spontaneous, and 15 evoked response bins (right ordinate.) Note that the top quarter of an octave is not included in any of the bins.(B and C) Firing rates of most neurons were low and followed a lognormal distribution.(B) Frequency histogram of nonzero spontaneous firing rates in individual octave bins (n = 567 octave bins, from 145 neurons). Each neuron contributed a maximum of four or five data points (because each neuron had four or five octave bins per epoch). The filled arrow shows the position of the median spontaneous firing rate, and the open arrow shows the position of the mean spontaneous firing rate.(C) The distribution of spontaneous firing rates (dots) was fit with a lognormal distribution (gray line), the mean and variance of which were given by the mean and variance of the original firing rate distribution (see Materials and Methods). The lognormal distribution appears as a normal distribution on a (semi-) logarithmic scale. The error bars show 95% confidence intervals determined by bootstrapping.
Mentions: We first analyzed the basic population response elicited by tones, beginning with the response to tones presented at 50 or 60 decibels (dB SPL). We divided the tone-evoked response into four 50-millisecond (ms) long “epochs”: spontaneous, early, late, and off (Figure 3A, also see Materials and Methods). To ensure a sufficient number of trials for assessing the statistical significance of putative changes in firing rate over background, we grouped responses across nearby frequencies (one-octave-wide bins; four- or five-octave bins for each response epoch). Control analyses using narrower (half-octave) bins gave similar results (see Materials and Methods), as expected from the relatively broad frequency tuning of neurons in the rat primary auditory cortex [22,23]; see also [24].

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
Related in: MedlinePlus