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Rapid Bidirectional Reorganization of Cortical Microcircuits.

Albieri G, Barnes SJ, de Celis Alonso B, Cheetham CE, Edwards CE, Lowe AS, Karunaratne H, Dear JP, Lee KC, Finnerty GT - Cereb. Cortex (2014)

Bottom Line: We found that there was rapid expansion followed by retraction of whisker cortical maps.Despite the rapid increase in local excitatory connectivity, the average strength and synaptic dynamics did not change, which suggests that new excitatory connections rapidly acquire the properties of established excitatory connections.Hence, the changes in local excitatory connectivity did not occur in all circuits involving pyramidal neurons.

View Article: PubMed Central - PubMed

Affiliation: MRC Centre for Neurodegeneration Research, King's College London, Institute of Psychiatry (Box44), London SE5 8AF, UK Current address: Division of Neurobiology, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK.

No MeSH data available.


Related in: MedlinePlus

Excitatory transmission onto L2/3 FS interneurons in deprived cortex is not affected by brief sensory deprivation. (A) Montage of maximum intensity projections from confocal z-stacks of an L2/3 FS interneuron filled with AF568 (orange). Scale bar, 40 μm. (B) Mean number of action potentials recorded in L2/3 FS interneurons evoked by 500 ms depolarizing current pulses in control (black) and deprived (red) cortex after 2–3 days of sensory deprivation. Inset: example trace of action potentials in an L2/3 FS interneuron evoked by a +0.4-nA current pulse (500 ms). Slope of the input–output curve: deprived, 182 ± 9 action potential nA−1, n = 26 FS interneurons; control, 186 ± 10 AP nA−1, n = 32 FS interneurons. Rheobase: deprived, 0.11 ± 0.04 nA, n = 26 FS interneurons; control, 0.19 ± 0.03 nA, n = 32 FS interneurons. (C) Pyr → FS connection: 20 Hz train of action potentials in the presynaptic pyramidal neuron evokes short latency uEPSPs (average 50 trials) in the postsynaptic FS interneuron. Scale bars: 20 mV (top), 0.5 mV (bottom), 50 ms. (D) Percentage of pyramidal cell to FS interneuron pairs (Pyr → FS) that were synaptically connected in control (black, 62%) and deprived (red, 62%) cortex. (E) Empirical distribution plots of mean uEPSP1 amplitudes in deprived (red) and control (black) cortex. Median [IQR] of mean uEPSP1 amplitudes for Pyr → FS connections: deprived, 1.34 [0.93–2.76] mV, n = 25; control, 1.24 [0.88–2.00] mV; n = 19. (F) Mean uEPSP amplitude during 20 Hz trains in deprived (red, n = 25 Pyr → FS connections) and control (black, n = 19 Pyr → FS connections) cortex. Error bars, SEM.
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BHU098F6: Excitatory transmission onto L2/3 FS interneurons in deprived cortex is not affected by brief sensory deprivation. (A) Montage of maximum intensity projections from confocal z-stacks of an L2/3 FS interneuron filled with AF568 (orange). Scale bar, 40 μm. (B) Mean number of action potentials recorded in L2/3 FS interneurons evoked by 500 ms depolarizing current pulses in control (black) and deprived (red) cortex after 2–3 days of sensory deprivation. Inset: example trace of action potentials in an L2/3 FS interneuron evoked by a +0.4-nA current pulse (500 ms). Slope of the input–output curve: deprived, 182 ± 9 action potential nA−1, n = 26 FS interneurons; control, 186 ± 10 AP nA−1, n = 32 FS interneurons. Rheobase: deprived, 0.11 ± 0.04 nA, n = 26 FS interneurons; control, 0.19 ± 0.03 nA, n = 32 FS interneurons. (C) Pyr → FS connection: 20 Hz train of action potentials in the presynaptic pyramidal neuron evokes short latency uEPSPs (average 50 trials) in the postsynaptic FS interneuron. Scale bars: 20 mV (top), 0.5 mV (bottom), 50 ms. (D) Percentage of pyramidal cell to FS interneuron pairs (Pyr → FS) that were synaptically connected in control (black, 62%) and deprived (red, 62%) cortex. (E) Empirical distribution plots of mean uEPSP1 amplitudes in deprived (red) and control (black) cortex. Median [IQR] of mean uEPSP1 amplitudes for Pyr → FS connections: deprived, 1.34 [0.93–2.76] mV, n = 25; control, 1.24 [0.88–2.00] mV; n = 19. (F) Mean uEPSP amplitude during 20 Hz trains in deprived (red, n = 25 Pyr → FS connections) and control (black, n = 19 Pyr → FS connections) cortex. Error bars, SEM.

Mentions: Although global inhibitory drive was not reduced, it remained possible that whisker deprivation induced disinhibition of a subset of inhibitory circuits. It has been proposed that inhibition undergoes plastic changes to maintain the balance between excitation and inhibition in reorganizing sensory cortex (Froemke et al. 2007; Marik et al. 2010; House et al. 2011; Vogels et al. 2011). Increasing local excitatory connectivity boosts positive feedback in cortical microcircuits and amplifies signals (Douglas et al. 1995). Recurrent excitatory circuits are usually counterbalanced by feedback inhibition to maintain network stability (Shu et al. 2003). Therefore, we reasoned that increased local excitatory connectivity may be matched by parallel changes in inhibition to maintain the excitatory–inhibitory balance. We recorded from FS interneurons (Fig. 6A; Methods) because they have been implicated in adult cortical plasticity (Pizzorusso et al. 2002; Ruediger et al. 2011; Campanac et al. 2013). It has been proposed that the excitatory–inhibitory balance can be maintained in the hippocampus by increased excitability of FS interneurons (Campanac et al. 2013). An increase in excitability would tend to boost inhibition, whereas decreased excitability would lead to disinhibition. Whisker deprivation alters the excitability of FS interneurons in L4 of deprived cortex during development (Sun 2009). Therefore, we tested whether whisker trimming for a few days altered the excitability of FS interneurons in L2/3 of deprived cortex. We found that there was no change in the slope of the input–output curve (deprived, 182 ± 9 AP nA−1, n = 26 FS interneurons; control, 186 ± 10 action potential (PA) nA−1, n = 32 FS interneurons; t = 0.291, P = 0.77, t-test), rheobase (deprived, 0.11 ± 0.04 nA, n = 26 FS interneurons; control, 0.19 ± 0.03 nA, n = 32 FS interneurons; t = 1.556, P = 0.125, t-test), or passive membrane properties of L2/3 FS interneurons (Fig. 6B and Supplementary Table 3). We concluded that the excitability of L2/3 FS interneurons was not affected by a few days of whisker deprivation.Figure 6.


Rapid Bidirectional Reorganization of Cortical Microcircuits.

Albieri G, Barnes SJ, de Celis Alonso B, Cheetham CE, Edwards CE, Lowe AS, Karunaratne H, Dear JP, Lee KC, Finnerty GT - Cereb. Cortex (2014)

Excitatory transmission onto L2/3 FS interneurons in deprived cortex is not affected by brief sensory deprivation. (A) Montage of maximum intensity projections from confocal z-stacks of an L2/3 FS interneuron filled with AF568 (orange). Scale bar, 40 μm. (B) Mean number of action potentials recorded in L2/3 FS interneurons evoked by 500 ms depolarizing current pulses in control (black) and deprived (red) cortex after 2–3 days of sensory deprivation. Inset: example trace of action potentials in an L2/3 FS interneuron evoked by a +0.4-nA current pulse (500 ms). Slope of the input–output curve: deprived, 182 ± 9 action potential nA−1, n = 26 FS interneurons; control, 186 ± 10 AP nA−1, n = 32 FS interneurons. Rheobase: deprived, 0.11 ± 0.04 nA, n = 26 FS interneurons; control, 0.19 ± 0.03 nA, n = 32 FS interneurons. (C) Pyr → FS connection: 20 Hz train of action potentials in the presynaptic pyramidal neuron evokes short latency uEPSPs (average 50 trials) in the postsynaptic FS interneuron. Scale bars: 20 mV (top), 0.5 mV (bottom), 50 ms. (D) Percentage of pyramidal cell to FS interneuron pairs (Pyr → FS) that were synaptically connected in control (black, 62%) and deprived (red, 62%) cortex. (E) Empirical distribution plots of mean uEPSP1 amplitudes in deprived (red) and control (black) cortex. Median [IQR] of mean uEPSP1 amplitudes for Pyr → FS connections: deprived, 1.34 [0.93–2.76] mV, n = 25; control, 1.24 [0.88–2.00] mV; n = 19. (F) Mean uEPSP amplitude during 20 Hz trains in deprived (red, n = 25 Pyr → FS connections) and control (black, n = 19 Pyr → FS connections) cortex. Error bars, SEM.
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BHU098F6: Excitatory transmission onto L2/3 FS interneurons in deprived cortex is not affected by brief sensory deprivation. (A) Montage of maximum intensity projections from confocal z-stacks of an L2/3 FS interneuron filled with AF568 (orange). Scale bar, 40 μm. (B) Mean number of action potentials recorded in L2/3 FS interneurons evoked by 500 ms depolarizing current pulses in control (black) and deprived (red) cortex after 2–3 days of sensory deprivation. Inset: example trace of action potentials in an L2/3 FS interneuron evoked by a +0.4-nA current pulse (500 ms). Slope of the input–output curve: deprived, 182 ± 9 action potential nA−1, n = 26 FS interneurons; control, 186 ± 10 AP nA−1, n = 32 FS interneurons. Rheobase: deprived, 0.11 ± 0.04 nA, n = 26 FS interneurons; control, 0.19 ± 0.03 nA, n = 32 FS interneurons. (C) Pyr → FS connection: 20 Hz train of action potentials in the presynaptic pyramidal neuron evokes short latency uEPSPs (average 50 trials) in the postsynaptic FS interneuron. Scale bars: 20 mV (top), 0.5 mV (bottom), 50 ms. (D) Percentage of pyramidal cell to FS interneuron pairs (Pyr → FS) that were synaptically connected in control (black, 62%) and deprived (red, 62%) cortex. (E) Empirical distribution plots of mean uEPSP1 amplitudes in deprived (red) and control (black) cortex. Median [IQR] of mean uEPSP1 amplitudes for Pyr → FS connections: deprived, 1.34 [0.93–2.76] mV, n = 25; control, 1.24 [0.88–2.00] mV; n = 19. (F) Mean uEPSP amplitude during 20 Hz trains in deprived (red, n = 25 Pyr → FS connections) and control (black, n = 19 Pyr → FS connections) cortex. Error bars, SEM.
Mentions: Although global inhibitory drive was not reduced, it remained possible that whisker deprivation induced disinhibition of a subset of inhibitory circuits. It has been proposed that inhibition undergoes plastic changes to maintain the balance between excitation and inhibition in reorganizing sensory cortex (Froemke et al. 2007; Marik et al. 2010; House et al. 2011; Vogels et al. 2011). Increasing local excitatory connectivity boosts positive feedback in cortical microcircuits and amplifies signals (Douglas et al. 1995). Recurrent excitatory circuits are usually counterbalanced by feedback inhibition to maintain network stability (Shu et al. 2003). Therefore, we reasoned that increased local excitatory connectivity may be matched by parallel changes in inhibition to maintain the excitatory–inhibitory balance. We recorded from FS interneurons (Fig. 6A; Methods) because they have been implicated in adult cortical plasticity (Pizzorusso et al. 2002; Ruediger et al. 2011; Campanac et al. 2013). It has been proposed that the excitatory–inhibitory balance can be maintained in the hippocampus by increased excitability of FS interneurons (Campanac et al. 2013). An increase in excitability would tend to boost inhibition, whereas decreased excitability would lead to disinhibition. Whisker deprivation alters the excitability of FS interneurons in L4 of deprived cortex during development (Sun 2009). Therefore, we tested whether whisker trimming for a few days altered the excitability of FS interneurons in L2/3 of deprived cortex. We found that there was no change in the slope of the input–output curve (deprived, 182 ± 9 AP nA−1, n = 26 FS interneurons; control, 186 ± 10 action potential (PA) nA−1, n = 32 FS interneurons; t = 0.291, P = 0.77, t-test), rheobase (deprived, 0.11 ± 0.04 nA, n = 26 FS interneurons; control, 0.19 ± 0.03 nA, n = 32 FS interneurons; t = 1.556, P = 0.125, t-test), or passive membrane properties of L2/3 FS interneurons (Fig. 6B and Supplementary Table 3). We concluded that the excitability of L2/3 FS interneurons was not affected by a few days of whisker deprivation.Figure 6.

Bottom Line: We found that there was rapid expansion followed by retraction of whisker cortical maps.Despite the rapid increase in local excitatory connectivity, the average strength and synaptic dynamics did not change, which suggests that new excitatory connections rapidly acquire the properties of established excitatory connections.Hence, the changes in local excitatory connectivity did not occur in all circuits involving pyramidal neurons.

View Article: PubMed Central - PubMed

Affiliation: MRC Centre for Neurodegeneration Research, King's College London, Institute of Psychiatry (Box44), London SE5 8AF, UK Current address: Division of Neurobiology, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK.

No MeSH data available.


Related in: MedlinePlus