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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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Primary mechanoreceptor afferent neurons do not show choice-related activity(a) Schematic of extracellular recording from mechanoreceptor neurons in the trigeminal ganglion (TG). (b) Example traces for Hit (blue), Miss (black) and Correct Rejection (red) trials. (c) Top: mean peri-stimulus spike time histograms (PSTHs; 4 ms bins; ± SEM) for n = 17 neurons. Bottom: mean of differences between Hit and Miss PSTHs for each neuron (magenta; mean ± 95% confidence interval). Gray traces: individual neurons. Arrows: stimulus onset. (d) Action potential (AP) rate evoked by the whisker stimulus is similar for Hit (blue circle, mean) and Miss (black circle) trials (p = 0.38, n = 17). Gray lines: individual neurons. (e) Pre-stimulus AP rate is similar for Hit and Miss trials (p = 0.55, two-tailed sign test, n = 17). Inset: cumulative histogram of same data. (f) Mean time course of detect probability (black) and stimulus probability (gray) across all TG recordings. Arrow: stimulus onset. n.s., p > 0.05;
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Figure 2: Primary mechanoreceptor afferent neurons do not show choice-related activity(a) Schematic of extracellular recording from mechanoreceptor neurons in the trigeminal ganglion (TG). (b) Example traces for Hit (blue), Miss (black) and Correct Rejection (red) trials. (c) Top: mean peri-stimulus spike time histograms (PSTHs; 4 ms bins; ± SEM) for n = 17 neurons. Bottom: mean of differences between Hit and Miss PSTHs for each neuron (magenta; mean ± 95% confidence interval). Gray traces: individual neurons. Arrows: stimulus onset. (d) Action potential (AP) rate evoked by the whisker stimulus is similar for Hit (blue circle, mean) and Miss (black circle) trials (p = 0.38, n = 17). Gray lines: individual neurons. (e) Pre-stimulus AP rate is similar for Hit and Miss trials (p = 0.55, two-tailed sign test, n = 17). Inset: cumulative histogram of same data. (f) Mean time course of detect probability (black) and stimulus probability (gray) across all TG recordings. Arrow: stimulus onset. n.s., p > 0.05;

Mentions: We sought to trace the origins of the choice-related activity we observed in primary somatosensory cortex. We began at the earliest possible stage: the primary mechanoreceptive afferents that transduce mechanical stimuli into action potentials. These neurons innervate the whisker follicle, have cell bodies located in the trigeminal ganglion, and send projections to somatosensory brainstem nuclei. Trigeminal ganglion neurons have single-whisker receptive fields27. We made extracellular recordings from single trigeminal ganglion neurons while mice performed the detection task using the single whisker in the neuron’s receptive field (Fig. 2). We analyzed spike rates during a baseline period, prior to the time of possible stimulus onset, and during a window shortly after the stimulus onset but prior to the typical reaction time on Go trials. Trigeminal ganglion neurons had low baseline spike rates that did not differ between Hit and Miss trials (0.77 ± 20.1 vs 0.62 ± 28.4 Hz [median ± interquartile range], p = 0.55, two-tailed sign test, n = 17; Fig. 2c,e), indicating that pre-stimulus activity in primary afferents was not a significant factor in perceptual outcome. Neurons were strongly driven by the whisker stimulus during both Hit and Miss trials (Fig. 2b,c). There was no difference in evoked rate between the two trial types (82.5 ± 9.2 vs 79.2 ± 9.9 Hz, p = 0.38; Fig. 2c,d).


Origins of choice-related activity in mouse somatosensory cortex.

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

Primary mechanoreceptor afferent neurons do not show choice-related activity(a) Schematic of extracellular recording from mechanoreceptor neurons in the trigeminal ganglion (TG). (b) Example traces for Hit (blue), Miss (black) and Correct Rejection (red) trials. (c) Top: mean peri-stimulus spike time histograms (PSTHs; 4 ms bins; ± SEM) for n = 17 neurons. Bottom: mean of differences between Hit and Miss PSTHs for each neuron (magenta; mean ± 95% confidence interval). Gray traces: individual neurons. Arrows: stimulus onset. (d) Action potential (AP) rate evoked by the whisker stimulus is similar for Hit (blue circle, mean) and Miss (black circle) trials (p = 0.38, n = 17). Gray lines: individual neurons. (e) Pre-stimulus AP rate is similar for Hit and Miss trials (p = 0.55, two-tailed sign test, n = 17). Inset: cumulative histogram of same data. (f) Mean time course of detect probability (black) and stimulus probability (gray) across all TG recordings. Arrow: stimulus onset. n.s., p > 0.05;
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Figure 2: Primary mechanoreceptor afferent neurons do not show choice-related activity(a) Schematic of extracellular recording from mechanoreceptor neurons in the trigeminal ganglion (TG). (b) Example traces for Hit (blue), Miss (black) and Correct Rejection (red) trials. (c) Top: mean peri-stimulus spike time histograms (PSTHs; 4 ms bins; ± SEM) for n = 17 neurons. Bottom: mean of differences between Hit and Miss PSTHs for each neuron (magenta; mean ± 95% confidence interval). Gray traces: individual neurons. Arrows: stimulus onset. (d) Action potential (AP) rate evoked by the whisker stimulus is similar for Hit (blue circle, mean) and Miss (black circle) trials (p = 0.38, n = 17). Gray lines: individual neurons. (e) Pre-stimulus AP rate is similar for Hit and Miss trials (p = 0.55, two-tailed sign test, n = 17). Inset: cumulative histogram of same data. (f) Mean time course of detect probability (black) and stimulus probability (gray) across all TG recordings. Arrow: stimulus onset. n.s., p > 0.05;
Mentions: We sought to trace the origins of the choice-related activity we observed in primary somatosensory cortex. We began at the earliest possible stage: the primary mechanoreceptive afferents that transduce mechanical stimuli into action potentials. These neurons innervate the whisker follicle, have cell bodies located in the trigeminal ganglion, and send projections to somatosensory brainstem nuclei. Trigeminal ganglion neurons have single-whisker receptive fields27. We made extracellular recordings from single trigeminal ganglion neurons while mice performed the detection task using the single whisker in the neuron’s receptive field (Fig. 2). We analyzed spike rates during a baseline period, prior to the time of possible stimulus onset, and during a window shortly after the stimulus onset but prior to the typical reaction time on Go trials. Trigeminal ganglion neurons had low baseline spike rates that did not differ between Hit and Miss trials (0.77 ± 20.1 vs 0.62 ± 28.4 Hz [median ± interquartile range], p = 0.55, two-tailed sign test, n = 17; Fig. 2c,e), indicating that pre-stimulus activity in primary afferents was not a significant factor in perceptual outcome. Neurons were strongly driven by the whisker stimulus during both Hit and Miss trials (Fig. 2b,c). There was no difference in evoked rate between the two trial types (82.5 ± 9.2 vs 79.2 ± 9.9 Hz, p = 0.38; Fig. 2c,d).

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