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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

New excitatory connections in deprived cortex have similar properties to control connections. (A) Schematic of recordings from pairs of synaptically connected L2/3 pyramidal neurons. (B) Mean uEPSP amplitudes in control cortex (black) and deprived cortex after 2–4 days (red) or 6–8 days (blue) of whisker trimming (2- to 4-day trim, 0.38 ± 0.11 mV, n = 16; 6- to 8-day trim, 0.11 ± 0.03 mV, n = 8; control, 0.43 ± 0.11 mV, n = 21). Inset: presynaptic action potential, postsynaptic EPSP. (C) Failure rates of neurotransmission between pyramidal neurons after 2–4 days (red) and 6–8 days (blue) of whisker trimming (median [IQR]: 2- to 4-day trim, 0.23 [0.00–0.49], n = 16; 6- to 8-day trim, 0.74 [0.56–0.85], n = 8; control, 0.05 [0.02–0.79], n = 19). Inset: presynaptic action potential, no postsynaptic response. (D) uEPSP amplitudes during a 20-Hz stimulus train in control cortex (filled circles) or deprived cortex after 2–4 days (red) and 6–8 days (blue) of whisker trimming. Error bars, SEM. Inset: 20 Hz train of postsynaptic EPSPs. (E) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 2–4 days trimming (red, n = 16) and in control cortex (black, n = 21). Error bars, SEM. (F) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 6–8 days trimming (blue, n = 8) and in control cortex (black, n = 21). Error bars, SEM. (G) Schematic shows sparse local connectivity in control cortex prior to whisker trimming (left panel). Whisker trimming for 3 days induces a rapid 3-fold increase in local excitatory connectivity (middle panel; new connections, red). Connectivity returns to control levels following 7 days of whisker trimming (right panel; 7-day trim connections, blue).
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BHU098F4: New excitatory connections in deprived cortex have similar properties to control connections. (A) Schematic of recordings from pairs of synaptically connected L2/3 pyramidal neurons. (B) Mean uEPSP amplitudes in control cortex (black) and deprived cortex after 2–4 days (red) or 6–8 days (blue) of whisker trimming (2- to 4-day trim, 0.38 ± 0.11 mV, n = 16; 6- to 8-day trim, 0.11 ± 0.03 mV, n = 8; control, 0.43 ± 0.11 mV, n = 21). Inset: presynaptic action potential, postsynaptic EPSP. (C) Failure rates of neurotransmission between pyramidal neurons after 2–4 days (red) and 6–8 days (blue) of whisker trimming (median [IQR]: 2- to 4-day trim, 0.23 [0.00–0.49], n = 16; 6- to 8-day trim, 0.74 [0.56–0.85], n = 8; control, 0.05 [0.02–0.79], n = 19). Inset: presynaptic action potential, no postsynaptic response. (D) uEPSP amplitudes during a 20-Hz stimulus train in control cortex (filled circles) or deprived cortex after 2–4 days (red) and 6–8 days (blue) of whisker trimming. Error bars, SEM. Inset: 20 Hz train of postsynaptic EPSPs. (E) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 2–4 days trimming (red, n = 16) and in control cortex (black, n = 21). Error bars, SEM. (F) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 6–8 days trimming (blue, n = 8) and in control cortex (black, n = 21). Error bars, SEM. (G) Schematic shows sparse local connectivity in control cortex prior to whisker trimming (left panel). Whisker trimming for 3 days induces a rapid 3-fold increase in local excitatory connectivity (middle panel; new connections, red). Connectivity returns to control levels following 7 days of whisker trimming (right panel; 7-day trim connections, blue).

Mentions: It remained possible that new connections were formed by single synapses and, hence, would have smaller uEPSP amplitudes and higher failure rates than pre-existing connections. However, we found that 2–4 days of whisker deprivation did not alter uEPSP amplitudes (deprived, 0.38 ± 0.11 mV, n = 16; control, 0.43 ± 0.11 mV, n = 21; P = 0.668, one-way ANOVA; Supplementary Table 1) (Fig. 4A,B) or EPSP failure rates (probability of failure—median [IQR]: control, 0.05 [0.02–0.79], n = 19 connections; 3-day trim, 0.23 [0.00–0.49], n = 16 connections; P = 0.517, Kolmogorov–Smirnov test) (Fig. 4C). In mature cortex, Pyr → Pyr connections in L2/3 show a mixture of facilitation and depression (Fig. 4D and Supplementary Fig. 5) (Cheetham et al. 2007). Comparison of the effects of whisker deprivation on the short-term synaptic dynamics is facilitated by normalization of the uEPSP amplitudes with respect to the first response in the train (uEPSP1) (Finnerty et al. 1999). We found that 2–4 days of whisker trimming did not affect the depression of the normalized steady-state amplitude when the presynaptic pyramidal neurons were stimulated to fire single action potentials at 20 Hz (Fig. 4E) (2- to 4-day trim, 0.87 ± 0.07, n = 16 connections; control, 0.88 ± 0.06, n = 21 connections; P = 0.163, one-way ANOVA). Our data show that new local excitatory connections with similar properties to control connections were formed within a few days in deprived cortex.Figure 4.


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)

New excitatory connections in deprived cortex have similar properties to control connections. (A) Schematic of recordings from pairs of synaptically connected L2/3 pyramidal neurons. (B) Mean uEPSP amplitudes in control cortex (black) and deprived cortex after 2–4 days (red) or 6–8 days (blue) of whisker trimming (2- to 4-day trim, 0.38 ± 0.11 mV, n = 16; 6- to 8-day trim, 0.11 ± 0.03 mV, n = 8; control, 0.43 ± 0.11 mV, n = 21). Inset: presynaptic action potential, postsynaptic EPSP. (C) Failure rates of neurotransmission between pyramidal neurons after 2–4 days (red) and 6–8 days (blue) of whisker trimming (median [IQR]: 2- to 4-day trim, 0.23 [0.00–0.49], n = 16; 6- to 8-day trim, 0.74 [0.56–0.85], n = 8; control, 0.05 [0.02–0.79], n = 19). Inset: presynaptic action potential, no postsynaptic response. (D) uEPSP amplitudes during a 20-Hz stimulus train in control cortex (filled circles) or deprived cortex after 2–4 days (red) and 6–8 days (blue) of whisker trimming. Error bars, SEM. Inset: 20 Hz train of postsynaptic EPSPs. (E) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 2–4 days trimming (red, n = 16) and in control cortex (black, n = 21). Error bars, SEM. (F) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 6–8 days trimming (blue, n = 8) and in control cortex (black, n = 21). Error bars, SEM. (G) Schematic shows sparse local connectivity in control cortex prior to whisker trimming (left panel). Whisker trimming for 3 days induces a rapid 3-fold increase in local excitatory connectivity (middle panel; new connections, red). Connectivity returns to control levels following 7 days of whisker trimming (right panel; 7-day trim connections, blue).
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BHU098F4: New excitatory connections in deprived cortex have similar properties to control connections. (A) Schematic of recordings from pairs of synaptically connected L2/3 pyramidal neurons. (B) Mean uEPSP amplitudes in control cortex (black) and deprived cortex after 2–4 days (red) or 6–8 days (blue) of whisker trimming (2- to 4-day trim, 0.38 ± 0.11 mV, n = 16; 6- to 8-day trim, 0.11 ± 0.03 mV, n = 8; control, 0.43 ± 0.11 mV, n = 21). Inset: presynaptic action potential, postsynaptic EPSP. (C) Failure rates of neurotransmission between pyramidal neurons after 2–4 days (red) and 6–8 days (blue) of whisker trimming (median [IQR]: 2- to 4-day trim, 0.23 [0.00–0.49], n = 16; 6- to 8-day trim, 0.74 [0.56–0.85], n = 8; control, 0.05 [0.02–0.79], n = 19). Inset: presynaptic action potential, no postsynaptic response. (D) uEPSP amplitudes during a 20-Hz stimulus train in control cortex (filled circles) or deprived cortex after 2–4 days (red) and 6–8 days (blue) of whisker trimming. Error bars, SEM. Inset: 20 Hz train of postsynaptic EPSPs. (E) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 2–4 days trimming (red, n = 16) and in control cortex (black, n = 21). Error bars, SEM. (F) Normalized uEPSP amplitudes of Pyr → Pyr connections during a 20-Hz train in deprived cortex after 6–8 days trimming (blue, n = 8) and in control cortex (black, n = 21). Error bars, SEM. (G) Schematic shows sparse local connectivity in control cortex prior to whisker trimming (left panel). Whisker trimming for 3 days induces a rapid 3-fold increase in local excitatory connectivity (middle panel; new connections, red). Connectivity returns to control levels following 7 days of whisker trimming (right panel; 7-day trim connections, blue).
Mentions: It remained possible that new connections were formed by single synapses and, hence, would have smaller uEPSP amplitudes and higher failure rates than pre-existing connections. However, we found that 2–4 days of whisker deprivation did not alter uEPSP amplitudes (deprived, 0.38 ± 0.11 mV, n = 16; control, 0.43 ± 0.11 mV, n = 21; P = 0.668, one-way ANOVA; Supplementary Table 1) (Fig. 4A,B) or EPSP failure rates (probability of failure—median [IQR]: control, 0.05 [0.02–0.79], n = 19 connections; 3-day trim, 0.23 [0.00–0.49], n = 16 connections; P = 0.517, Kolmogorov–Smirnov test) (Fig. 4C). In mature cortex, Pyr → Pyr connections in L2/3 show a mixture of facilitation and depression (Fig. 4D and Supplementary Fig. 5) (Cheetham et al. 2007). Comparison of the effects of whisker deprivation on the short-term synaptic dynamics is facilitated by normalization of the uEPSP amplitudes with respect to the first response in the train (uEPSP1) (Finnerty et al. 1999). We found that 2–4 days of whisker trimming did not affect the depression of the normalized steady-state amplitude when the presynaptic pyramidal neurons were stimulated to fire single action potentials at 20 Hz (Fig. 4E) (2- to 4-day trim, 0.87 ± 0.07, n = 16 connections; control, 0.88 ± 0.06, n = 21 connections; P = 0.163, one-way ANOVA). Our data show that new local excitatory connections with similar properties to control connections were formed within a few days in deprived cortex.Figure 4.

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