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Origins of choice-related activity in mouse somatosensory cortex.

Yang H, Kwon SE, Severson KS, O'Connor DH - Nat. Neurosci. (2015)

Bottom Line: Spike trains from primary mechanoreceptive neurons did not predict choices about identical stimuli.An intracellular measure of stimulus sensitivity determined which neurons converted choice-related depolarization into spiking.Our results reveal how choice-related spiking emerges across neural circuits and within single neurons.

View Article: PubMed Central - PubMed

Affiliation: The Solomon H. Snyder Department of Neuroscience and Brain Science Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

ABSTRACT
During perceptual decisions about faint or ambiguous sensory stimuli, even identical stimuli can produce different choices. Spike trains from sensory cortex neurons can predict trial-to-trial variability in choice. Choice-related spiking is widely studied as a way to link cortical activity to perception, but its origins remain unclear. Using imaging and electrophysiology, we found that mouse primary somatosensory cortex neurons showed robust choice-related activity during a tactile detection task. Spike trains from primary mechanoreceptive neurons did not predict choices about identical stimuli. Spike trains from thalamic relay neurons showed highly transient, weak choice-related activity. Intracellular recordings in cortex revealed a prolonged choice-related depolarization in most neurons that was not accounted for by feed-forward thalamic input. Top-down axons projecting from secondary to primary somatosensory cortex signaled choice. An intracellular measure of stimulus sensitivity determined which neurons converted choice-related depolarization into spiking. Our results reveal how choice-related spiking emerges across neural circuits and within single neurons.

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Related in: MedlinePlus

Choice-related membrane potential dynamics in S1 cortex(a) Top: Schematic of intracellular (whole cell) recording in primary somatosensory (barrel) cortex. Bottom: Example membrane potential (Vm) traces for Hit (blue) and Miss (black) trials. (b) Removing spikes from Vm traces. Top: example raw Vm traces; action potentials (APs; shown truncated) are evident in the Hit and Miss trials. Bottom: the same Vm traces after median filtering and smoothing to eliminate APs. Arrows: stimulus onset for Hit and Miss traces. (c) Top: Mean Vm change after AP removal (± SEM; n = 22 neurons) for Hit (blue), Miss (black) and Correct Rejection (red) trials. Bottom: Mean of differences between mean Vm on Hits and mean Vm on Misses (magenta; mean ± 95% confidence interval; n = 22 neurons). Gray traces: individual recordings. (d) Left: Stimulus-evoked change in membrane potential (ΔVm) is larger on Hit trials compared with Miss trials (p < 1e–3, two-tailed sign test, n = 22). Right: Histogram of the mean difference in ΔVm between Hits and Misses for each neuron (arrow: mean at 1.4 mV). (e) Pre-stimulus membrane potential dynamics are similar for Hit and Miss trials, both mean Vm (p = 0.13, n = 22) and standard deviation of Vm (p = 0.64). (f) Histograms of detect probability (black) and stimulus probability (gray) computed from ΔVm. Magenta: means ± 95% confidence intervals. (g) Mean time course of detect probability (black) and stimulus probability (gray) across Vm recordings (n = 22). VPM detect probability is shown for comparison (cyan, same data as in Fig. 3g). (h) Extracting action potential times from Vm traces. Top: Example Vm traces from an S1 neuron for Hits, Misses and Correct Rejections. Bottom: action potential rasters obtained from the example traces. (i) Mean time course of detect probability and stimulus probability calculated using action potential times instead of Vm, across the top third of neurons ranked by DP (n = 7, corresponding to purple plot symbols in panel (j)). (j) Left: detect probability calculated for each neuron using either action potential rate (y-axis) or evoked change in membrane potential (x-axis). Right: stimulus probability calculated for each neuron using either action potential rate or evoked change in membrane potential. Neurons that did not spike had y-axis values set to 0.5. Purple symbols: neurons included in traces in (i). n.s., p > 0.05; ***, p < 0.001.
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Figure 5: Choice-related membrane potential dynamics in S1 cortex(a) Top: Schematic of intracellular (whole cell) recording in primary somatosensory (barrel) cortex. Bottom: Example membrane potential (Vm) traces for Hit (blue) and Miss (black) trials. (b) Removing spikes from Vm traces. Top: example raw Vm traces; action potentials (APs; shown truncated) are evident in the Hit and Miss trials. Bottom: the same Vm traces after median filtering and smoothing to eliminate APs. Arrows: stimulus onset for Hit and Miss traces. (c) Top: Mean Vm change after AP removal (± SEM; n = 22 neurons) for Hit (blue), Miss (black) and Correct Rejection (red) trials. Bottom: Mean of differences between mean Vm on Hits and mean Vm on Misses (magenta; mean ± 95% confidence interval; n = 22 neurons). Gray traces: individual recordings. (d) Left: Stimulus-evoked change in membrane potential (ΔVm) is larger on Hit trials compared with Miss trials (p < 1e–3, two-tailed sign test, n = 22). Right: Histogram of the mean difference in ΔVm between Hits and Misses for each neuron (arrow: mean at 1.4 mV). (e) Pre-stimulus membrane potential dynamics are similar for Hit and Miss trials, both mean Vm (p = 0.13, n = 22) and standard deviation of Vm (p = 0.64). (f) Histograms of detect probability (black) and stimulus probability (gray) computed from ΔVm. Magenta: means ± 95% confidence intervals. (g) Mean time course of detect probability (black) and stimulus probability (gray) across Vm recordings (n = 22). VPM detect probability is shown for comparison (cyan, same data as in Fig. 3g). (h) Extracting action potential times from Vm traces. Top: Example Vm traces from an S1 neuron for Hits, Misses and Correct Rejections. Bottom: action potential rasters obtained from the example traces. (i) Mean time course of detect probability and stimulus probability calculated using action potential times instead of Vm, across the top third of neurons ranked by DP (n = 7, corresponding to purple plot symbols in panel (j)). (j) Left: detect probability calculated for each neuron using either action potential rate (y-axis) or evoked change in membrane potential (x-axis). Right: stimulus probability calculated for each neuron using either action potential rate or evoked change in membrane potential. Neurons that did not spike had y-axis values set to 0.5. Purple symbols: neurons included in traces in (i). n.s., p > 0.05; ***, p < 0.001.

Mentions: Intracellular recording, recently possible in task-performing animals19,32,33, reveals the subthreshold membrane potential (Vm) dynamics that govern spiking. To investigate the transformation of thalamic and other synaptic inputs into choice-related spiking, we made intracellular (whole cell) recordings from non-fast-spiking cortical neurons across all layers (n = 22) during our detection task (Fig. 5a; Supplementary Fig. 5). We used intrinsic signal imaging (Methods) to target recordings to the cortical column representing the whisker used to solve the task.


Origins of choice-related activity in mouse somatosensory cortex.

Yang H, Kwon SE, Severson KS, O'Connor DH - Nat. Neurosci. (2015)

Choice-related membrane potential dynamics in S1 cortex(a) Top: Schematic of intracellular (whole cell) recording in primary somatosensory (barrel) cortex. Bottom: Example membrane potential (Vm) traces for Hit (blue) and Miss (black) trials. (b) Removing spikes from Vm traces. Top: example raw Vm traces; action potentials (APs; shown truncated) are evident in the Hit and Miss trials. Bottom: the same Vm traces after median filtering and smoothing to eliminate APs. Arrows: stimulus onset for Hit and Miss traces. (c) Top: Mean Vm change after AP removal (± SEM; n = 22 neurons) for Hit (blue), Miss (black) and Correct Rejection (red) trials. Bottom: Mean of differences between mean Vm on Hits and mean Vm on Misses (magenta; mean ± 95% confidence interval; n = 22 neurons). Gray traces: individual recordings. (d) Left: Stimulus-evoked change in membrane potential (ΔVm) is larger on Hit trials compared with Miss trials (p < 1e–3, two-tailed sign test, n = 22). Right: Histogram of the mean difference in ΔVm between Hits and Misses for each neuron (arrow: mean at 1.4 mV). (e) Pre-stimulus membrane potential dynamics are similar for Hit and Miss trials, both mean Vm (p = 0.13, n = 22) and standard deviation of Vm (p = 0.64). (f) Histograms of detect probability (black) and stimulus probability (gray) computed from ΔVm. Magenta: means ± 95% confidence intervals. (g) Mean time course of detect probability (black) and stimulus probability (gray) across Vm recordings (n = 22). VPM detect probability is shown for comparison (cyan, same data as in Fig. 3g). (h) Extracting action potential times from Vm traces. Top: Example Vm traces from an S1 neuron for Hits, Misses and Correct Rejections. Bottom: action potential rasters obtained from the example traces. (i) Mean time course of detect probability and stimulus probability calculated using action potential times instead of Vm, across the top third of neurons ranked by DP (n = 7, corresponding to purple plot symbols in panel (j)). (j) Left: detect probability calculated for each neuron using either action potential rate (y-axis) or evoked change in membrane potential (x-axis). Right: stimulus probability calculated for each neuron using either action potential rate or evoked change in membrane potential. Neurons that did not spike had y-axis values set to 0.5. Purple symbols: neurons included in traces in (i). n.s., p > 0.05; ***, p < 0.001.
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Figure 5: Choice-related membrane potential dynamics in S1 cortex(a) Top: Schematic of intracellular (whole cell) recording in primary somatosensory (barrel) cortex. Bottom: Example membrane potential (Vm) traces for Hit (blue) and Miss (black) trials. (b) Removing spikes from Vm traces. Top: example raw Vm traces; action potentials (APs; shown truncated) are evident in the Hit and Miss trials. Bottom: the same Vm traces after median filtering and smoothing to eliminate APs. Arrows: stimulus onset for Hit and Miss traces. (c) Top: Mean Vm change after AP removal (± SEM; n = 22 neurons) for Hit (blue), Miss (black) and Correct Rejection (red) trials. Bottom: Mean of differences between mean Vm on Hits and mean Vm on Misses (magenta; mean ± 95% confidence interval; n = 22 neurons). Gray traces: individual recordings. (d) Left: Stimulus-evoked change in membrane potential (ΔVm) is larger on Hit trials compared with Miss trials (p < 1e–3, two-tailed sign test, n = 22). Right: Histogram of the mean difference in ΔVm between Hits and Misses for each neuron (arrow: mean at 1.4 mV). (e) Pre-stimulus membrane potential dynamics are similar for Hit and Miss trials, both mean Vm (p = 0.13, n = 22) and standard deviation of Vm (p = 0.64). (f) Histograms of detect probability (black) and stimulus probability (gray) computed from ΔVm. Magenta: means ± 95% confidence intervals. (g) Mean time course of detect probability (black) and stimulus probability (gray) across Vm recordings (n = 22). VPM detect probability is shown for comparison (cyan, same data as in Fig. 3g). (h) Extracting action potential times from Vm traces. Top: Example Vm traces from an S1 neuron for Hits, Misses and Correct Rejections. Bottom: action potential rasters obtained from the example traces. (i) Mean time course of detect probability and stimulus probability calculated using action potential times instead of Vm, across the top third of neurons ranked by DP (n = 7, corresponding to purple plot symbols in panel (j)). (j) Left: detect probability calculated for each neuron using either action potential rate (y-axis) or evoked change in membrane potential (x-axis). Right: stimulus probability calculated for each neuron using either action potential rate or evoked change in membrane potential. Neurons that did not spike had y-axis values set to 0.5. Purple symbols: neurons included in traces in (i). n.s., p > 0.05; ***, p < 0.001.
Mentions: Intracellular recording, recently possible in task-performing animals19,32,33, reveals the subthreshold membrane potential (Vm) dynamics that govern spiking. To investigate the transformation of thalamic and other synaptic inputs into choice-related spiking, we made intracellular (whole cell) recordings from non-fast-spiking cortical neurons across all layers (n = 22) during our detection task (Fig. 5a; Supplementary Fig. 5). We used intrinsic signal imaging (Methods) to target recordings to the cortical column representing the whisker used to solve the task.

Bottom Line: Spike trains from primary mechanoreceptive neurons did not predict choices about identical stimuli.An intracellular measure of stimulus sensitivity determined which neurons converted choice-related depolarization into spiking.Our results reveal how choice-related spiking emerges across neural circuits and within single neurons.

View Article: PubMed Central - PubMed

Affiliation: The Solomon H. Snyder Department of Neuroscience and Brain Science Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

ABSTRACT
During perceptual decisions about faint or ambiguous sensory stimuli, even identical stimuli can produce different choices. Spike trains from sensory cortex neurons can predict trial-to-trial variability in choice. Choice-related spiking is widely studied as a way to link cortical activity to perception, but its origins remain unclear. Using imaging and electrophysiology, we found that mouse primary somatosensory cortex neurons showed robust choice-related activity during a tactile detection task. Spike trains from primary mechanoreceptive neurons did not predict choices about identical stimuli. Spike trains from thalamic relay neurons showed highly transient, weak choice-related activity. Intracellular recordings in cortex revealed a prolonged choice-related depolarization in most neurons that was not accounted for by feed-forward thalamic input. Top-down axons projecting from secondary to primary somatosensory cortex signaled choice. An intracellular measure of stimulus sensitivity determined which neurons converted choice-related depolarization into spiking. Our results reveal how choice-related spiking emerges across neural circuits and within single neurons.

Show MeSH
Related in: MedlinePlus