Facilitation of long-term potentiation in layer II/III horizontal connections of rat motor cortex following layer I stimulation: route of effect and cholinergic contributions
G. Hess et Jp. Donoghue, Facilitation of long-term potentiation in layer II/III horizontal connections of rat motor cortex following layer I stimulation: route of effect and cholinergic contributions, EXP BRAIN R, 127(3), 1999, pp. 279-290
The ability of layer I activation to facilitate the induction of long-term
potentiation (LTP) in layer II/III horizontal connections of motor cortex (
MI) was examined in rat brain slice preparations. Field potentials evoked i
n layer I and layer II/III horizontal pathways were recorded from radially
aligned MI sites. While theta burst stimulation (TBS) of layer II/III pathw
ays alone failed to induce LTP, simultaneous TBS of layer I and layer II/II
I inputs on alternate sides of the recording electrodes induced LTP in the
layer II/III input in 8 out of 13 slices (mean change +20+/-6%; N=13). In t
he same cases, the layer I connections showed mixed effects: LTP in three c
ases, LTD in five cases, and no modification in five slices. Despite the fa
cilitatory effect of layer I activation on layer II/III LTP induction, we f
ound that the critical circuitry for this effect was outside layer I. Cutti
ng the layer I fibers selectively in the slice did not prevent layer II/III
LTP induction, while cuts preserving only layer I blocked layer II/III LTP
after conjoint I+II/III TBS. Cholinergic fibers were evaluated as candidat
es for the facilitatory effect because they branch widely in both layers an
d they are thought to participate in synaptic modification. The cholinergic
contribution to layer II/III LTP facilitation was investigated using bath
application of muscarinic antagonists. Muscarinic blockade prevented facili
tation of layer II/III LTP by layer I coactivation. Instead, conjoint stimu
lation in 10 mu M atropine produced long-term depression (LTD) of layer II/
III (-18+/-9%; N=11) as well as of layer I(-21+/-6%; N=11) horizontal respo
nses. These results indicate that connections formed within layer I are ine
ffective in promoting LTP in the deeper-lying horizontal connections; the c
ritical route by which layer I stimulation influenced LTP induction require
d the circuitry in the deeper layers, particularly the cholinergic system.
Thus, it appears that diffuse cholinergic afferents provide an additional r
oute to regulate activity-dependent synaptic modificaton in horizontal cort
ical connections.