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Experience-Dependent, Layer-Specific Development of Divergent Thalamocortical Connectivity.

Crocker-Buque A, Brown SM, Kind PC, Isaac JT, Daw MI - Cereb. Cortex (2014)

Bottom Line: Here, we show that, in neonates, the input to layer 6 is as strong as that to layer 4.This strengthening consists of an increase in axon branching and the divergence of connectivity in layer 4 without a change in the strength of individual connections.We propose that experience-driven LTP stabilizes transient TC synapses in layer 4 to increase strength and divergence specifically in layer 4 over layer 6.

View Article: PubMed Central - PubMed

Affiliation: Centre for Integrative Physiology, University of Edinburgh, Edinburgh, UK.

No MeSH data available.


Increase in the proportion of L4 cells contacted by single TC axons with age. (A) Example experiment with 2 simultaneously recorded L4 cells during minimal TC stimulation. Traces show responses in cell 1 (black) and cell 2 (gray) to TC stimulation at intensity indicated. Lower panel shows amplitude and stimulus intensity versus trial no. plot for both cells. Note the failures in cell 2 on trials producing EPSCs in cell 1. (B) EPSC versus EPSC plot for all trials involving 2 cells shown in A (black circles no EPSC, gray circles EPSC in cell 1 only, and open circles EPSC in both cells). (C) As for A but 2 cells respond to same trial stimuli. (D) EPSC versus EPSC plot for all trials involving 2 cells shown in C (black circles no EPSC and open circles EPSC in both cells). (E) Bar graph showing the proportion of cell pairs responding to the same trials during minimal stimulation versus age. *P < 0.05.
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BHU031F5: Increase in the proportion of L4 cells contacted by single TC axons with age. (A) Example experiment with 2 simultaneously recorded L4 cells during minimal TC stimulation. Traces show responses in cell 1 (black) and cell 2 (gray) to TC stimulation at intensity indicated. Lower panel shows amplitude and stimulus intensity versus trial no. plot for both cells. Note the failures in cell 2 on trials producing EPSCs in cell 1. (B) EPSC versus EPSC plot for all trials involving 2 cells shown in A (black circles no EPSC, gray circles EPSC in cell 1 only, and open circles EPSC in both cells). (C) As for A but 2 cells respond to same trial stimuli. (D) EPSC versus EPSC plot for all trials involving 2 cells shown in C (black circles no EPSC and open circles EPSC in both cells). (E) Bar graph showing the proportion of cell pairs responding to the same trials during minimal stimulation versus age. *P < 0.05.

Mentions: We next tested the remaining possibility that selective strengthening of TC to L4 input is due to individual TC axons contacting a greater number of cells in L4. We took advantage of the high release probability to make the assumption that when a single axon is activated by minimal stimulation, an EPSC will be observed in all postsynaptic cells on almost every trial. We made simultaneous whole-cell recordings from 2 neighboring L4 cells and applied a minimal stimulation protocol to determine whether the same axon contacted each cell. Figure 5A,B shows an experiment in which the lowest stimulation intensity to evoke an EPSC in cell 1 failed to evoke an EPSC in cell 2. Successes in cell 1 coincide with failures in cell 2, which can be clearly seen when EPSC amplitude in cell 1 is plotted against that in cell 2 (gray circles in Fig. 5B). EPSCs are seen in cell 2 only with significantly higher stimulus intensity. In contrast, Figure 5C,D shows an experiment in which the same trials always produced either EPSCs or failures in both cells; here, the EPSC–EPSC plot shows that there are no trials that produce an EPSC in only one cell. Such recordings strongly suggest that the same axon makes synaptic contacts onto both recorded cells. The proportion of cell pairs contacted by the same axon increase sharply at the end of the first week with no further increase by P19–P21 (P3–P5 1/11, 9% pairs; P6–P7 2/9, 22% pairs; P8–P9 6/11, 55% pairs, P = 0.01 vs. P3–P5, P19–P21 5/12, 42% pairs, P = 0.04 vs. P3–P5, P = 0.27 vs. P8–P9; Fig. 5E); thus, an increase in the number of L4 cells functionally contacted by each TC axon in the absence of a change in the synaptic weight contributed by each axon is associated with the relative increase in TC input to L4 in the first postnatal week. To investigate TC connectivity to L6 cells, we recorded from 2 L6 cells simultaneously during minimal stimulation. Coincident EPSCs were never observed in 2 L6 cells (P3–P5 n = 13; P6–P7 n = 12; P8–P9 n = 14; P19–P21 n = 11) presumably because of low connectivity. As such it is not possible to conclude whether there is a change in the proportion of L6 cells contacted by each TC axon with development.Figure 5.


Experience-Dependent, Layer-Specific Development of Divergent Thalamocortical Connectivity.

Crocker-Buque A, Brown SM, Kind PC, Isaac JT, Daw MI - Cereb. Cortex (2014)

Increase in the proportion of L4 cells contacted by single TC axons with age. (A) Example experiment with 2 simultaneously recorded L4 cells during minimal TC stimulation. Traces show responses in cell 1 (black) and cell 2 (gray) to TC stimulation at intensity indicated. Lower panel shows amplitude and stimulus intensity versus trial no. plot for both cells. Note the failures in cell 2 on trials producing EPSCs in cell 1. (B) EPSC versus EPSC plot for all trials involving 2 cells shown in A (black circles no EPSC, gray circles EPSC in cell 1 only, and open circles EPSC in both cells). (C) As for A but 2 cells respond to same trial stimuli. (D) EPSC versus EPSC plot for all trials involving 2 cells shown in C (black circles no EPSC and open circles EPSC in both cells). (E) Bar graph showing the proportion of cell pairs responding to the same trials during minimal stimulation versus age. *P < 0.05.
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BHU031F5: Increase in the proportion of L4 cells contacted by single TC axons with age. (A) Example experiment with 2 simultaneously recorded L4 cells during minimal TC stimulation. Traces show responses in cell 1 (black) and cell 2 (gray) to TC stimulation at intensity indicated. Lower panel shows amplitude and stimulus intensity versus trial no. plot for both cells. Note the failures in cell 2 on trials producing EPSCs in cell 1. (B) EPSC versus EPSC plot for all trials involving 2 cells shown in A (black circles no EPSC, gray circles EPSC in cell 1 only, and open circles EPSC in both cells). (C) As for A but 2 cells respond to same trial stimuli. (D) EPSC versus EPSC plot for all trials involving 2 cells shown in C (black circles no EPSC and open circles EPSC in both cells). (E) Bar graph showing the proportion of cell pairs responding to the same trials during minimal stimulation versus age. *P < 0.05.
Mentions: We next tested the remaining possibility that selective strengthening of TC to L4 input is due to individual TC axons contacting a greater number of cells in L4. We took advantage of the high release probability to make the assumption that when a single axon is activated by minimal stimulation, an EPSC will be observed in all postsynaptic cells on almost every trial. We made simultaneous whole-cell recordings from 2 neighboring L4 cells and applied a minimal stimulation protocol to determine whether the same axon contacted each cell. Figure 5A,B shows an experiment in which the lowest stimulation intensity to evoke an EPSC in cell 1 failed to evoke an EPSC in cell 2. Successes in cell 1 coincide with failures in cell 2, which can be clearly seen when EPSC amplitude in cell 1 is plotted against that in cell 2 (gray circles in Fig. 5B). EPSCs are seen in cell 2 only with significantly higher stimulus intensity. In contrast, Figure 5C,D shows an experiment in which the same trials always produced either EPSCs or failures in both cells; here, the EPSC–EPSC plot shows that there are no trials that produce an EPSC in only one cell. Such recordings strongly suggest that the same axon makes synaptic contacts onto both recorded cells. The proportion of cell pairs contacted by the same axon increase sharply at the end of the first week with no further increase by P19–P21 (P3–P5 1/11, 9% pairs; P6–P7 2/9, 22% pairs; P8–P9 6/11, 55% pairs, P = 0.01 vs. P3–P5, P19–P21 5/12, 42% pairs, P = 0.04 vs. P3–P5, P = 0.27 vs. P8–P9; Fig. 5E); thus, an increase in the number of L4 cells functionally contacted by each TC axon in the absence of a change in the synaptic weight contributed by each axon is associated with the relative increase in TC input to L4 in the first postnatal week. To investigate TC connectivity to L6 cells, we recorded from 2 L6 cells simultaneously during minimal stimulation. Coincident EPSCs were never observed in 2 L6 cells (P3–P5 n = 13; P6–P7 n = 12; P8–P9 n = 14; P19–P21 n = 11) presumably because of low connectivity. As such it is not possible to conclude whether there is a change in the proportion of L6 cells contacted by each TC axon with development.Figure 5.

Bottom Line: Here, we show that, in neonates, the input to layer 6 is as strong as that to layer 4.This strengthening consists of an increase in axon branching and the divergence of connectivity in layer 4 without a change in the strength of individual connections.We propose that experience-driven LTP stabilizes transient TC synapses in layer 4 to increase strength and divergence specifically in layer 4 over layer 6.

View Article: PubMed Central - PubMed

Affiliation: Centre for Integrative Physiology, University of Edinburgh, Edinburgh, UK.

No MeSH data available.