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Effects of isoflurane anesthesia on ensemble patterns of Ca2+ activity in mouse v1: reduced direction selectivity independent of increased correlations in cellular activity.

Goltstein PM, Montijn JS, Pennartz CM - PLoS ONE (2015)

Bottom Line: As compared to anesthesia, populations of V1 neurons coded more mutual information on opposite stimulus directions during wakefulness, whereas information on stimulus orientation differences was lower.Increases in correlations of calcium activity during visual stimulation were correlated with poorer population coding, which raised the hypothesis that the anesthesia-induced increase in correlations may be causal to degrading directional coding.The population-wide decrease in coding for stimulus direction thus occurs independently of anesthesia-induced increments in correlations of spontaneous activity.

View Article: PubMed Central - PubMed

Affiliation: Center for Neuroscience, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands; Research Priority Program Brain and Cognition, University of Amsterdam, Amsterdam, The Netherlands.

ABSTRACT
Anesthesia affects brain activity at the molecular, neuronal and network level, but it is not well-understood how tuning properties of sensory neurons and network connectivity change under its influence. Using in vivo two-photon calcium imaging we matched neuron identity across episodes of wakefulness and anesthesia in the same mouse and recorded spontaneous and visually evoked activity patterns of neuronal ensembles in these two states. Correlations in spontaneous patterns of calcium activity between pairs of neurons were increased under anesthesia. While orientation selectivity remained unaffected by anesthesia, this treatment reduced direction selectivity, which was attributable to an increased response to the -direction. As compared to anesthesia, populations of V1 neurons coded more mutual information on opposite stimulus directions during wakefulness, whereas information on stimulus orientation differences was lower. Increases in correlations of calcium activity during visual stimulation were correlated with poorer population coding, which raised the hypothesis that the anesthesia-induced increase in correlations may be causal to degrading directional coding. Visual stimulation under anesthesia, however, decorrelated ongoing activity patterns to a level comparable to wakefulness. Because visual stimulation thus appears to 'break' the strength of pairwise correlations normally found in spontaneous activity under anesthesia, the changes in correlational structure cannot explain the awake-anesthesia difference in direction coding. The population-wide decrease in coding for stimulus direction thus occurs independently of anesthesia-induced increments in correlations of spontaneous activity.

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Pairwise correlations in cellular calcium signals during visual stimulation.(A) Correlation between calcium time series of all simultaneously recorded pairs of orientation tuned neurons during spontaneous activity or visual stimulation, studied under awake (Aw) and anesthetized (An) conditions (*** p < 10–10). (B) Pairwise correlations during visual stimulation as a function of spatial distance between cell bodies of orientation tuned neurons (Yellow: Awake, r = -0.10, p = 0.0026; Blue: Anesthesia, r = -0.077, p = 0.026; n = 846). (C) Pairwise correlations during visual stimulation as a function of the difference in preferred direction of orientation tuned neurons (Yellow: Awake, r = -0.14, p = 4.0 * 10–5; Blue: Anesthesia, r = -0.075, p < 0.028; n = 846).
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pone.0118277.g006: Pairwise correlations in cellular calcium signals during visual stimulation.(A) Correlation between calcium time series of all simultaneously recorded pairs of orientation tuned neurons during spontaneous activity or visual stimulation, studied under awake (Aw) and anesthetized (An) conditions (*** p < 10–10). (B) Pairwise correlations during visual stimulation as a function of spatial distance between cell bodies of orientation tuned neurons (Yellow: Awake, r = -0.10, p = 0.0026; Blue: Anesthesia, r = -0.077, p = 0.026; n = 846). (C) Pairwise correlations during visual stimulation as a function of the difference in preferred direction of orientation tuned neurons (Yellow: Awake, r = -0.14, p = 4.0 * 10–5; Blue: Anesthesia, r = -0.075, p < 0.028; n = 846).

Mentions: We observed an inverse relationship between correlations during visual stimulation and decoding of population activity, especially for opposite stimulus directions (Fig. 5C7), which may be taken to suggest that increased redundancy, as gauged by pairwise correlations, could at least partly underlie the reduction in direction coding. Surprisingly, the data do not support this view. Although under anesthesia neurons are more responsive to the direction (Fig. 3E) and showed higher correlations in spontaneous activity (Fig. 2), overall pairwise correlations in calcium activity of orientation-tuned neurons did not significantly differ between the awake and anesthetized state during visual stimulation (WMPSR test, p = 0.092; n = 846; Fig. 6A). Rather, anesthesia revealed a significant decorrelation when comparing calcium activity during visual stimulation with spontaneous calcium activity (WMPSR test, p < 10–10; n = 846; Fig. 6A, dark blue and cyan bar). In awake animals, no such decline was observed (WMPSR test, P = 0.94; n = 846), which suggests that the cortical network was already in a decorrelated state during spontaneous activity.


Effects of isoflurane anesthesia on ensemble patterns of Ca2+ activity in mouse v1: reduced direction selectivity independent of increased correlations in cellular activity.

Goltstein PM, Montijn JS, Pennartz CM - PLoS ONE (2015)

Pairwise correlations in cellular calcium signals during visual stimulation.(A) Correlation between calcium time series of all simultaneously recorded pairs of orientation tuned neurons during spontaneous activity or visual stimulation, studied under awake (Aw) and anesthetized (An) conditions (*** p < 10–10). (B) Pairwise correlations during visual stimulation as a function of spatial distance between cell bodies of orientation tuned neurons (Yellow: Awake, r = -0.10, p = 0.0026; Blue: Anesthesia, r = -0.077, p = 0.026; n = 846). (C) Pairwise correlations during visual stimulation as a function of the difference in preferred direction of orientation tuned neurons (Yellow: Awake, r = -0.14, p = 4.0 * 10–5; Blue: Anesthesia, r = -0.075, p < 0.028; n = 846).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4338011&req=5

pone.0118277.g006: Pairwise correlations in cellular calcium signals during visual stimulation.(A) Correlation between calcium time series of all simultaneously recorded pairs of orientation tuned neurons during spontaneous activity or visual stimulation, studied under awake (Aw) and anesthetized (An) conditions (*** p < 10–10). (B) Pairwise correlations during visual stimulation as a function of spatial distance between cell bodies of orientation tuned neurons (Yellow: Awake, r = -0.10, p = 0.0026; Blue: Anesthesia, r = -0.077, p = 0.026; n = 846). (C) Pairwise correlations during visual stimulation as a function of the difference in preferred direction of orientation tuned neurons (Yellow: Awake, r = -0.14, p = 4.0 * 10–5; Blue: Anesthesia, r = -0.075, p < 0.028; n = 846).
Mentions: We observed an inverse relationship between correlations during visual stimulation and decoding of population activity, especially for opposite stimulus directions (Fig. 5C7), which may be taken to suggest that increased redundancy, as gauged by pairwise correlations, could at least partly underlie the reduction in direction coding. Surprisingly, the data do not support this view. Although under anesthesia neurons are more responsive to the direction (Fig. 3E) and showed higher correlations in spontaneous activity (Fig. 2), overall pairwise correlations in calcium activity of orientation-tuned neurons did not significantly differ between the awake and anesthetized state during visual stimulation (WMPSR test, p = 0.092; n = 846; Fig. 6A). Rather, anesthesia revealed a significant decorrelation when comparing calcium activity during visual stimulation with spontaneous calcium activity (WMPSR test, p < 10–10; n = 846; Fig. 6A, dark blue and cyan bar). In awake animals, no such decline was observed (WMPSR test, P = 0.94; n = 846), which suggests that the cortical network was already in a decorrelated state during spontaneous activity.

Bottom Line: As compared to anesthesia, populations of V1 neurons coded more mutual information on opposite stimulus directions during wakefulness, whereas information on stimulus orientation differences was lower.Increases in correlations of calcium activity during visual stimulation were correlated with poorer population coding, which raised the hypothesis that the anesthesia-induced increase in correlations may be causal to degrading directional coding.The population-wide decrease in coding for stimulus direction thus occurs independently of anesthesia-induced increments in correlations of spontaneous activity.

View Article: PubMed Central - PubMed

Affiliation: Center for Neuroscience, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands; Research Priority Program Brain and Cognition, University of Amsterdam, Amsterdam, The Netherlands.

ABSTRACT
Anesthesia affects brain activity at the molecular, neuronal and network level, but it is not well-understood how tuning properties of sensory neurons and network connectivity change under its influence. Using in vivo two-photon calcium imaging we matched neuron identity across episodes of wakefulness and anesthesia in the same mouse and recorded spontaneous and visually evoked activity patterns of neuronal ensembles in these two states. Correlations in spontaneous patterns of calcium activity between pairs of neurons were increased under anesthesia. While orientation selectivity remained unaffected by anesthesia, this treatment reduced direction selectivity, which was attributable to an increased response to the -direction. As compared to anesthesia, populations of V1 neurons coded more mutual information on opposite stimulus directions during wakefulness, whereas information on stimulus orientation differences was lower. Increases in correlations of calcium activity during visual stimulation were correlated with poorer population coding, which raised the hypothesis that the anesthesia-induced increase in correlations may be causal to degrading directional coding. Visual stimulation under anesthesia, however, decorrelated ongoing activity patterns to a level comparable to wakefulness. Because visual stimulation thus appears to 'break' the strength of pairwise correlations normally found in spontaneous activity under anesthesia, the changes in correlational structure cannot explain the awake-anesthesia difference in direction coding. The population-wide decrease in coding for stimulus direction thus occurs independently of anesthesia-induced increments in correlations of spontaneous activity.

Show MeSH
Related in: MedlinePlus