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Journal of Neuroscience, Vol 11, 1800-1809, Copyright © 1991 by Society for Neuroscience
Synaptic physiology of horizontal connections in the cat's visual cortex
JA Hirsch and CD Gilbert
Laboratory of Neurobiology, Rockefeller University, New York, New York 10021.
Horizontal connections are a principal component of intrinsic cortical
circuitry. They arise mainly from pyramidal cells and course parallel to
the brain's surface for distances as long as 8 mm, linking columns with
shared orientation preference and allowing cells to integrate visual
information from outside their receptive fields. We examined the synaptic
physiology of the horizontal pathway in slices of the cat's striate cortex
and found that activating lateral fibers produced both excitation and
inhibition. We recorded the postsynaptic responses of identified pyramidal
cells in layer 2 + 3 of area 17 to electrical shocks applied at three
sites: in the home column of the impaled neuron either in layer 2 + 3 or 4,
or at a lateral distance of 0.9-3 mm in layer 2 + 3. Within the home
column, suprathreshold stimuli produced compound EPSPs with action
potentials, followed by fast, GABAAergic IPSPs and a slower, GABABergic
IPSP. For the distant stimulating site, the threshold response was an EPSP.
Stronger shocks frequently evoked a disynaptic, GABAAergic IPSP that
truncated the EPSP and could dominate the postsynaptic response. At the
resting potential, the horizontally evoked EPSP was too small to elicit
spikes. With depolarization of the membrane, however, it grew several
hundred-fold. This amplification was blocked by
N-(2,6-dimethylphenylcarbamoylmethyl)triethylammonium bromide (QX-314), but
not by 2-amino-5-phosphonovalerate (APV), indicating that it was mediated
by Na+ channels, rather than by NMDA receptors. We propose that the
horizontal connections provide the means for stimuli outside the receptive
field to modulate activity elicited within its confines. The
voltage-dependent enhancement of the laterally evoked EPSP may explain why
stimulating the surround by itself fails to drive cells but can facilitate
their response to stimuli within the receptive field. The ability to
initiate disynaptic inhibition from lateral sites shows that recruiting
appropriate groups of horizontal fibers can also have a suppressive effect.
Thus, the effect of horizontal input is state dependent, with the size and
sign of the laterally evoked response changing according to the balance of
converging inputs.
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|
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|
|
|
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|
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|
|
|
|
|
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|
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|
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[Full Text]
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|
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|
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|
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|
|
|
|
|
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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18(19):
7972 - 7986.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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18(11):
4403 - 4416.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. R. Sheth, C. I. Moore, and M. Sur
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J Neurophysiol,
January 1, 1998;
79(1):
464 - 470.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Cash and R. Yuste
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J. Neurosci.,
January 1, 1998;
18(1):
10 - 15.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Varela, K. Sen, J. Gibson, J. Fost, L. F. Abbott, and S. B. Nelson
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J. Neurosci.,
October 15, 1997;
17(20):
7926 - 7940.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. J. Berman, J. Plant, R. W. Turner, and L. Maler
Excitatory Amino Acid Receptors at a Feedback Pathway in the Electrosensory System: Implications for the Searchlight Hypothesis
J Neurophysiol,
October 1, 1997;
78(4):
1869 - 1881.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Adini, D. Sagi, and M. Tsodyks
Excitatory-inhibitory network in the visual cortex: Psychophysical evidence
PNAS,
September 16, 1997;
94(19):
10426 - 10431.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. K. Seamans, N. A. Gorelova, and C. R. Yang
Contributions of Voltage-Gated Ca2+ Channels in the Proximal versus Distal Dendrites to Synaptic Integration in Prefrontal Cortical Neurons
J. Neurosci.,
August 1, 1997;
17(15):
5936 - 5948.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Shao and A. Burkhalter
Different Balance of Excitation and Inhibition in Forward and Feedback Circuits of Rat Visual Cortex
J. Neurosci.,
November 15, 1996;
16(22):
7353 - 7365.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. C. Katz and C. J. Shatz
Synaptic Activity and the Construction of Cortical Circuits
Science,
November 15, 1996;
274(5290):
1133 - 1138.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
Z. Gil and Y. Amitai
Properties of Convergent Thalamocortical and Intracortical Synaptic Potentials in Single Neurons of Neocortex
J. Neurosci.,
October 15, 1996;
16(20):
6567 - 6578.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C.D. Gilbert, A. Das, M. Ito, M.K. Kapadia, and G. Westheimer
Cortical Dynamics and Visual Perception
Cold Spring Harb Symp Quant Biol,
January 1, 1996;
61(0):
105 - 113.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M Stemmler, M Usher, and E Niebur
Lateral interactions in primary visual cortex: a model bridging physiology and psychophysics
Science,
September 29, 1995;
269(5232):
1877 - 1880.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M Tanifuji, T Sugiyama, and K Murase
Horizontal propagation of excitation in rat visual cortical slices revealed by optical imaging
Science,
November 11, 1994;
266(5187):
1057 - 1059.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. Azouz and C. M. Gray
Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo
PNAS,
July 5, 2000;
97(14):
8110 - 8115.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J. Physiol.,
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540(1):
335 - 350.
[Abstract]
[Full Text]
[PDF]
|
|
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|
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