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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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Intracellular stimulus sensitivity predicts choice-related spiking(a) Biophysical properties related to excitability, including spike threshold (Vspike), resting membrane potential (Vrest) or their difference, do not explain the magnitude of detect probability. (b) Example reversal potential (Vrev) calculation. Vrev quantifies the relationship between the amplitude of stimulus-evoked postsynaptic potentials and pre-stimulus membrane potential. Left: example traces of Vm. Gray shading indicates windows used to measure pre-stimulus Vm and evoked PSP (arrow: stimulus onset). Right: PSP amplitude plotted against pre-stimulus Vm shows a linear relationship. Reversal potential, Vrev, is defined as the pre-stimulus Vm that produces a zero amplitude PSP. Vrev for this neuron is −51.8 mV. Magenta, yellow and black points correspond to traces in left panel. (c) Spike rate detect probability (left) and stimulus probability (right) are strongly correlated with the difference between reversal potential and spike threshold (R2 = 0.6, p = 0.001). Plot symbol color indicates nominal cortical layer (estimated by depth). (d) Detect probability and stimulus probability tend to be higher in the same neurons. Two-dimensional histogram showing correlated detect and stimulus probability (R2 = 0.14, p < 1e–3) across populations of S1 layer 2/3 neurons (n = 1,746 neurons from 6 mice).
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Figure 7: Intracellular stimulus sensitivity predicts choice-related spiking(a) Biophysical properties related to excitability, including spike threshold (Vspike), resting membrane potential (Vrest) or their difference, do not explain the magnitude of detect probability. (b) Example reversal potential (Vrev) calculation. Vrev quantifies the relationship between the amplitude of stimulus-evoked postsynaptic potentials and pre-stimulus membrane potential. Left: example traces of Vm. Gray shading indicates windows used to measure pre-stimulus Vm and evoked PSP (arrow: stimulus onset). Right: PSP amplitude plotted against pre-stimulus Vm shows a linear relationship. Reversal potential, Vrev, is defined as the pre-stimulus Vm that produces a zero amplitude PSP. Vrev for this neuron is −51.8 mV. Magenta, yellow and black points correspond to traces in left panel. (c) Spike rate detect probability (left) and stimulus probability (right) are strongly correlated with the difference between reversal potential and spike threshold (R2 = 0.6, p = 0.001). Plot symbol color indicates nominal cortical layer (estimated by depth). (d) Detect probability and stimulus probability tend to be higher in the same neurons. Two-dimensional histogram showing correlated detect and stimulus probability (R2 = 0.14, p < 1e–3) across populations of S1 layer 2/3 neurons (n = 1,746 neurons from 6 mice).

Mentions: First, we asked whether three biophysical quantities that affect neuronal excitability could explain which neurons showed choice-related spiking: (1) Vspike, the membrane potential at which a spike is initiated; (2) Vrest, resting membrane potential; (3) Vrest − Vspike, which sets the amplitude of depolarization necessary to cause a spike. Surprisingly, none of these simple measures of excitability correlated with spike rate detect probability (Fig. 7a).


Origins of choice-related activity in mouse somatosensory cortex.

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

Intracellular stimulus sensitivity predicts choice-related spiking(a) Biophysical properties related to excitability, including spike threshold (Vspike), resting membrane potential (Vrest) or their difference, do not explain the magnitude of detect probability. (b) Example reversal potential (Vrev) calculation. Vrev quantifies the relationship between the amplitude of stimulus-evoked postsynaptic potentials and pre-stimulus membrane potential. Left: example traces of Vm. Gray shading indicates windows used to measure pre-stimulus Vm and evoked PSP (arrow: stimulus onset). Right: PSP amplitude plotted against pre-stimulus Vm shows a linear relationship. Reversal potential, Vrev, is defined as the pre-stimulus Vm that produces a zero amplitude PSP. Vrev for this neuron is −51.8 mV. Magenta, yellow and black points correspond to traces in left panel. (c) Spike rate detect probability (left) and stimulus probability (right) are strongly correlated with the difference between reversal potential and spike threshold (R2 = 0.6, p = 0.001). Plot symbol color indicates nominal cortical layer (estimated by depth). (d) Detect probability and stimulus probability tend to be higher in the same neurons. Two-dimensional histogram showing correlated detect and stimulus probability (R2 = 0.14, p < 1e–3) across populations of S1 layer 2/3 neurons (n = 1,746 neurons from 6 mice).
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4696889&req=5

Figure 7: Intracellular stimulus sensitivity predicts choice-related spiking(a) Biophysical properties related to excitability, including spike threshold (Vspike), resting membrane potential (Vrest) or their difference, do not explain the magnitude of detect probability. (b) Example reversal potential (Vrev) calculation. Vrev quantifies the relationship between the amplitude of stimulus-evoked postsynaptic potentials and pre-stimulus membrane potential. Left: example traces of Vm. Gray shading indicates windows used to measure pre-stimulus Vm and evoked PSP (arrow: stimulus onset). Right: PSP amplitude plotted against pre-stimulus Vm shows a linear relationship. Reversal potential, Vrev, is defined as the pre-stimulus Vm that produces a zero amplitude PSP. Vrev for this neuron is −51.8 mV. Magenta, yellow and black points correspond to traces in left panel. (c) Spike rate detect probability (left) and stimulus probability (right) are strongly correlated with the difference between reversal potential and spike threshold (R2 = 0.6, p = 0.001). Plot symbol color indicates nominal cortical layer (estimated by depth). (d) Detect probability and stimulus probability tend to be higher in the same neurons. Two-dimensional histogram showing correlated detect and stimulus probability (R2 = 0.14, p < 1e–3) across populations of S1 layer 2/3 neurons (n = 1,746 neurons from 6 mice).
Mentions: First, we asked whether three biophysical quantities that affect neuronal excitability could explain which neurons showed choice-related spiking: (1) Vspike, the membrane potential at which a spike is initiated; (2) Vrest, resting membrane potential; (3) Vrest − Vspike, which sets the amplitude of depolarization necessary to cause a spike. Surprisingly, none of these simple measures of excitability correlated with spike rate detect probability (Fig. 7a).

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