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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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Sound-Evoked Responses in the Unanesthetized Auditory Cortex Are Heterogeneous(A–H) Tone-evoked responses in the auditory cortex of unanesthetized rats are heterogeneous. The panels show response dynamics of eight representative neurons to 60-dB tones. In each panel, dots represent individual spikes, the gray shaded region indicates the tone duration (100 ms). (A) transient onset response; (B) suppressive response; (C) transient onset response followed by sustained excitatory response followed by off response; (D) late onset response followed by strong off response; (E) late onset response; (F) off response; (G) sustained response combined with suppressive response; (H) non-responsive cell. See also Figures S4–S8 for more examples.(I) Example of single neuron responses to 54-dB sweeps. Dots represent individual spikes, the gray shaded regions indicate the stimulus duration.(J) Example of single neuron responses to natural sound (Knudsen's frog). Spectrogram of stimulus is shown at top (red indicated highest intensities and blue indicates lowest intensities), and individual trials are plotted in the middle (ticks represent spikes). Firing rate curve in the bottom of the panel was computed by first summing the spikes in 20-ms bins and then convolving the resulting peristimulus time histogram (PSTH) with a Gaussian (σ = 20 ms). Note the long time scale compared to the other panels.
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pbio-0060016-g002: Sound-Evoked Responses in the Unanesthetized Auditory Cortex Are Heterogeneous(A–H) Tone-evoked responses in the auditory cortex of unanesthetized rats are heterogeneous. The panels show response dynamics of eight representative neurons to 60-dB tones. In each panel, dots represent individual spikes, the gray shaded region indicates the tone duration (100 ms). (A) transient onset response; (B) suppressive response; (C) transient onset response followed by sustained excitatory response followed by off response; (D) late onset response followed by strong off response; (E) late onset response; (F) off response; (G) sustained response combined with suppressive response; (H) non-responsive cell. See also Figures S4–S8 for more examples.(I) Example of single neuron responses to 54-dB sweeps. Dots represent individual spikes, the gray shaded regions indicate the stimulus duration.(J) Example of single neuron responses to natural sound (Knudsen's frog). Spectrogram of stimulus is shown at top (red indicated highest intensities and blue indicates lowest intensities), and individual trials are plotted in the middle (ticks represent spikes). Firing rate curve in the bottom of the panel was computed by first summing the spikes in 20-ms bins and then convolving the resulting peristimulus time histogram (PSTH) with a Gaussian (σ = 20 ms). Note the long time scale compared to the other panels.

Mentions: Figure 2 shows some examples of the range of response types we observed. In one neuron (Figure 2A), tones elicited a transient, short latency response of the sort commonly observed in the barbiturate-anesthetized auditory cortex. In a second neuron (Figure 2B), tones elicited a suppression of background activity. In a third neuron (Figure 2C), higher frequency tones (∼8–40 kilohertz [kHz]) elicited vigorous sustained firing; interestingly, lower-frequency tones elicited transient responses in the same neuron, emphasizing that the distinction between “transient” and “sustained” applies to responses, not neurons. Other more complex response patterns were also observed (Figure 2D–2G.) Finally, half of the neurons tested (50%, see below) showed no change in firing rate for any stimulus presented (Figure 2H). Because a given neuron could show very different response patterns to stimuli of different frequencies (e.g., Figure 2C), we could not find a simple and objective scheme for organizing neurons into a small number of distinct classes, such as “transient,” “sustained,” “off,” etc. The neurons shown in Figure 2 are a subset; the complete set of responses from the entire dataset is shown in the Figures S4–S8.


Sparse representation of sounds in the unanesthetized auditory cortex.

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

Sound-Evoked Responses in the Unanesthetized Auditory Cortex Are Heterogeneous(A–H) Tone-evoked responses in the auditory cortex of unanesthetized rats are heterogeneous. The panels show response dynamics of eight representative neurons to 60-dB tones. In each panel, dots represent individual spikes, the gray shaded region indicates the tone duration (100 ms). (A) transient onset response; (B) suppressive response; (C) transient onset response followed by sustained excitatory response followed by off response; (D) late onset response followed by strong off response; (E) late onset response; (F) off response; (G) sustained response combined with suppressive response; (H) non-responsive cell. See also Figures S4–S8 for more examples.(I) Example of single neuron responses to 54-dB sweeps. Dots represent individual spikes, the gray shaded regions indicate the stimulus duration.(J) Example of single neuron responses to natural sound (Knudsen's frog). Spectrogram of stimulus is shown at top (red indicated highest intensities and blue indicates lowest intensities), and individual trials are plotted in the middle (ticks represent spikes). Firing rate curve in the bottom of the panel was computed by first summing the spikes in 20-ms bins and then convolving the resulting peristimulus time histogram (PSTH) with a Gaussian (σ = 20 ms). Note the long time scale compared to the other panels.
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pbio-0060016-g002: Sound-Evoked Responses in the Unanesthetized Auditory Cortex Are Heterogeneous(A–H) Tone-evoked responses in the auditory cortex of unanesthetized rats are heterogeneous. The panels show response dynamics of eight representative neurons to 60-dB tones. In each panel, dots represent individual spikes, the gray shaded region indicates the tone duration (100 ms). (A) transient onset response; (B) suppressive response; (C) transient onset response followed by sustained excitatory response followed by off response; (D) late onset response followed by strong off response; (E) late onset response; (F) off response; (G) sustained response combined with suppressive response; (H) non-responsive cell. See also Figures S4–S8 for more examples.(I) Example of single neuron responses to 54-dB sweeps. Dots represent individual spikes, the gray shaded regions indicate the stimulus duration.(J) Example of single neuron responses to natural sound (Knudsen's frog). Spectrogram of stimulus is shown at top (red indicated highest intensities and blue indicates lowest intensities), and individual trials are plotted in the middle (ticks represent spikes). Firing rate curve in the bottom of the panel was computed by first summing the spikes in 20-ms bins and then convolving the resulting peristimulus time histogram (PSTH) with a Gaussian (σ = 20 ms). Note the long time scale compared to the other panels.
Mentions: Figure 2 shows some examples of the range of response types we observed. In one neuron (Figure 2A), tones elicited a transient, short latency response of the sort commonly observed in the barbiturate-anesthetized auditory cortex. In a second neuron (Figure 2B), tones elicited a suppression of background activity. In a third neuron (Figure 2C), higher frequency tones (∼8–40 kilohertz [kHz]) elicited vigorous sustained firing; interestingly, lower-frequency tones elicited transient responses in the same neuron, emphasizing that the distinction between “transient” and “sustained” applies to responses, not neurons. Other more complex response patterns were also observed (Figure 2D–2G.) Finally, half of the neurons tested (50%, see below) showed no change in firing rate for any stimulus presented (Figure 2H). Because a given neuron could show very different response patterns to stimuli of different frequencies (e.g., Figure 2C), we could not find a simple and objective scheme for organizing neurons into a small number of distinct classes, such as “transient,” “sustained,” “off,” etc. The neurons shown in Figure 2 are a subset; the complete set of responses from the entire dataset is shown in the Figures S4–S8.

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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