Plasticity of horizontal connections at a functional border in adult rat somatosensory cortex

Abstract

Horizontal connections in superficial cortical layers integrate information across sensory maps by connecting related functional columns. It has been hypothesized that these connections mediate cortical reorganization via synaptic plasticity. However, it is not known if the horizontal connections from discontinuous cortical regions can undergo plasticity in the adult. Here we located the border between two discontinuous cortical representations in vivo and used either pairing or low-frequency stimulation to induce synaptic plasticity in the horizontal connections surrounding this border in vitro. Individual neurons revealed significant and diverse forms of synaptic plasticity for horizontal connections within a continuous representation and discontinuous representations. Interestingly, both enhancement and depression were observed following both plasticity paradigms. Furthermore, plasticity was not restricted by the border's presence. Depolarization in the absence of synaptic stimulation also produced synaptic plasticity, but with different characteristics. These experiments suggest that plasticity of horizontal connections may mediate functional reorganization.

Figure 1

The in vivo and in vitro preparations. (a) Lateral view of the rat brain with a schematic map of S1 overlaid. The gray circle depicts one location of forepaw/lower jaw border. Recordings were made in vivo to determine the location of the border and the border was marked with DiI. (b) Schematic of in vitro slice recording. The top solid line depicts pia and the bottom solid line depicts white matter, the border is the vertical thin line, and the border marked with DiI is the thin oval. The recording electrode recorded from a single neuron (triangle) approximately 100 μm from the marked border (black oval) and two stimulating electrodes were placed at the same depth from the pia at 300 μm from the tip of the recording electrode for continuous representation (gray square) and discontinuous representation stimulation (black square). Layer four was undercut (dashed line) in order to isolate the horizontal connections.

Figure 2

Changes in PSP amplitude generated by one pathway pairing. (a) Sixteen neurons underwent pairing of continuous representation connections only. (b) Fourteen neurons underwent pairing of discontinuous representation connections only. (1) Schematic of pathway pairing paradigm. (2) Example responses from a cell in which pairing of the indicated pathway induced homosynaptic (a) or homo- and heterosynaptic (b) enhancement of the pathways. Traces are averaged over five minutes. Grey traces are averaged PSPs from before pairing (baseline) and the black traces are averaged PSPs from 20 minutes postpairing. (3): % change of PSP amplitude over time for the cell shown in (2). PSP amplitude change was averaged over five minute intervals.

Figure 3

LTP induced by a pairing paradigm given to both continuous representation and discontinuous representation pathways. (a) Schematic drawing of the pairing protocol. Both pathways are paired alternately to induce synaptic plasticity. (b) Example of PSPs from a cell where both pathways underwent LTP. Gray traces are averaged baseline PSPs. Black traces are averaged traces 20 minutes postpairing. Traces are averaged over 5 minutes (15 traces) for both pre- and postpairing PSPs, (c) % change of PSP amplitude over time for the cell shown in 2. PSP amplitude change was averaged over five minute intervals.

Figure 4

Individual neuron data. (a) Continuous pathway pairing. Change in PSP amplitude (expressed as percent of the baseline PSP amplitude) for continuous representation pathway plotted against discontinuous representation pathway for each cell that received continuous pathway pairing. Solid diagonal line depicts slope of one. Dashed lines depict 15% above and below no change (100%). (b) Discontinuous pathway pairing. Change in PSP amplitude (expressed as percent of the baseline PSP amplitude) for continuous representation pathway plotted against discontinuous representation pathway for each cell that received discontinuous representation pathway pairing. Conventions are as in (a). (c) Both pathway pairing. Change in PSP amplitude (expressed as percent of the baseline PSP amplitude) for continuous representation plotted against discontinuous representation pathway for each cell that received both pathway pairing. Conventions are as in (a).

Figure 5

APV blocks pairing induced LTP. (a) Schematic of the two-pathway pairing paradigm. (b) Example responses from a cell that was treated with APV; gray traces are averaged baseline PSPs. Black traces are averaged traces 20 minutes postpairing. Traces are averaged over 5 minutes (15 traces) for both pre- and postpairing PSPs. No enhancement occurred following pairing of both continuous representation and discontinuous representation pathways. (c) Change in PSP amplitude for the continuous representation pathway plotted against discontinuous representation for each cell that received APV and both pathway pairing. Solid diagonal line depicts slope of one. Dashed lines depict 15% above and below no change.

Figure 6

LTP of neurons that received depolarization without synaptic stimulation. (a) Schematic of connections. No pairing was given, only robust depolarization. (b) Example of PSPs. Gray traces are averaged baseline PSPs. Black traces are averaged traces 20 minutes postpairing. Traces are averaged over 5 minutes (15 traces) for both pre- and postpairing PSPs. (c) % change of PSP amplitude over time for the cell shown in 2. PSP amplitude change was averaged over five minute intervals. (d). Individual data: change in PSP amplitude (expressed as percent of the baseline PSP amplitude) for continuous representation plotted against discontinuous representation pathway for each cell that received depolarization only. Conventions are as in Figure 4.

Figure 7

LFS induced plasticity. (a) Fourteen neurons underwent LFS to the continuous representation connections only. (b) Twelve neurons underwent LFS of discontinuous representation connections only. (1) Schematic drawing of the in vitro preparation. (2) Example responses from sample cells. Traces are averaged over five minutes with grey showing PSPs from before pairing (baseline) and black showing those from 20 minutes postpairing. (3): % change of PSP amplitude over time for the cell shown in (2). PSP amplitude change was averaged over five minute intervals. (4) Change in PSP amplitude (expressed as percent of the baseline PSP amplitude) for continuous representation pathway plotted against discontinuous representation pathway for each cell. Solid diagonal line depicts slope of one. Dashed lines depict 15% above and below no change (100%).