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Journal of Neuroscience, Vol 15, 5324-5333, Copyright © 1995 by Society for Neuroscience
Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex
MA Castro-Alamancos, JP Donoghue and BW Connors
Department of Neuroscience, Brown University, Providence, Rhode Island 02912, USA.
We have studied vertical synaptic pathways in two cytoarchitectonically
distinct areas of rat neocortex--the granular primary somatosensory (SI)
area and the agranular primary motor (MI) area--and tested their propensity
to generate long-term potentiation (LTP), long-term depression (LTD), and
related forms of synaptic plasticity. Extracellular and intracellular
responses were recorded in layer II/III of slices in vitro while
stimulating in middle cortical layers (in or around layer IV). Under
control conditions, 5 Hz theta-burst stimulation produced LTP in the
granular area, but not in the agranular area. Agranular cortex did generate
short-term potentiation that decayed within 20 min. Varying the inter-burst
frequency from 2 Hz to 10 Hz reliably yielded LTP of 21-34% above control
levels in granular cortex, but no lasting changes were induced in agranular
cortex. However, the agranular cortex was capable of generating LTP if a
GABAA receptor antagonist was applied locally at the recording site during
the induction phase. In contrast to LTP, an identical form of homosynaptic
LTD could be induced in both granular and agranular areas by applying low
frequency stimulation (1 Hz for 15 min) to the middle layers. Under control
conditions, both LTP and LTD were synapse- specific; theta-burst or
low-frequency stimulation in the vertical pathway did not induce changes in
responses to stimulation of a layer II/III horizontal pathway. Application
of the NMDA receptor antagonist D-2-amino-5-phosphonovaleric acid (AP5)
blocked the induction of both LTP and LTD in granular and agranular cortex.
In the presence of AP5, low-frequency conditioning stimuli yielded a
short-term depression in both areas that decayed within 10-15 min.
Nifedipine, which blocks L- type, voltage-sensitive calcium channels,
slightly depressed the magnitudes of LTP and LTD but did not abolish them.
Synaptic responses evoked during theta-burst stimulation were strikingly
different in granular and agranular areas. Responses in granular cortex
were progressively facilitated during each sequence of 10 theta-bursts, and
from sequence-to-sequence; in contrast, responses in agranular cortex were
stable during an entire theta-burst tetanus. The results suggest that
vertical pathways in primary somatosensory cortex and primary motor cortex
express several forms of synaptic plasticity. They were equally capable of
generating LTD, but the pathways in somatosensory cortex much more reliably
generated LTP, unless inhibition was reduced. LTP may be more easily
produced in sensory cortex because of the pronounced synaptic facilitation
that occurs there during repetitive stimulation of the induction
phase.(ABSTRACT TRUNCATED AT 400 WORDS)
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