Download Department of Neurophysiology, Institute of

Tohoku
J. exp.
Med.,
1974,
Effects
of Thalamic
Lateral
Geniculate
of
Principal
114, 227-240
Midline
Nuclei
Transmission
Cells
and
Excitation
Stimulation
in
Rats
of
upon
: Inhibition
Internuncial
Cells
ICHIJI
SUMITOMO
Department of Neurophysiology, Institute of Higher Nervous
Activity, Osaka University Medical School, Osaka
SUMITOMO,
I. Effects of Thalamic Midline Nuclei Stimulation upon Lateral
Geniculate Transmission in Rats: Inhibition of Principal Cells and Excitation of
Internuncial Cells. Tohoku J. exp. Med., 1974, 114 (3), 227-240Effects
of low-frequency stimulation of thalamic midline nuclei .(MID) upon unitary
activities of principal (P) and internuncial (I) cells of the lateral geniculate body
were examined in urethane-anesthetized rats. P-cells responsed to single shocks
to the optic tract (OT) with single spikes at short latencies (initial spike, IS),
followed by a phase of inhibition which lasted for more than 150 msec and ended
with a burst of grouped discharges (late discharge, LD). Excitability of P-cells,
assessed with the response probability of IS to testing OT shocks, was reduced for
about 300 msec after single shock stimulation of MID. Usually this excitability
depression became evident about 20 msec after MID shocks and was maximum
from 50 to 100 msec. LDs were made more vigorous when MID shocks were given
almost simultaneously with testing OT shocks. This was interpreted that MID
stimulation induced an inhibition in P-cells and it summed with that induced
by OT stimulation. That the MID-induced inhibition of P-cells was due to
IPSPs was proved by the quasi-intracellular recording. I-cells, the units fired
repetitively by single OT shocks and have been presumed to be inhibitory neurons
acting upon P-cells, were found to receive from MID stimulation an excitatory
effect followed by an inhibitory one of long duration. It was suggested that the
primary inhibition of P-cells by low-frequency stimulation of MID would be a
direct consequence of the primary excitation of I-cells.
thalamic midline nuclei; lateral geniculate body; principal cells; internuncial cells
Synaptic transmission at the lateral geniculate body (LGB) is known to be
facilitated by high-frequency electric stimulation of the midbrain reticular formation
(Long 1959; Steriade and Demetrescu 1960; Arden and Soderberg 1961; Suzuki and
Taira 1961; Okuda 1962; Ogawa 1963; Fukuda and Iwama 1971; Doty et al. 1973).
Using the rat, Fukuda and Iwama (1971) showed that facilitation of the LGB relay
cells (principal cells, P-cells) was always associated with inhibition of the internuncial
cells (I-cells) which were claimed to be inhibitory neurons acting upon P-cells (Burke
and Sefton 1966a, b, c). From these findings Fukuda and Iwama (1971) concluded
that the reticular facilitation of the LGB synaptic transmission might be resulted
Received
for publication,
July
2, 1974.
227
228
from
I. Sumitomo
inhibition
of the
inhibitory
interneurons.
In this paper, it will be shown first that low-frequency stimulation of thalamic
midline nuclei (MID) suppresses activity of P-cells in the rat LGB, and secondly,
evidence will be presented that the same stimulation resulted in excitation of I-cells.
Combining these results with Fukuda and Iwama's finding (1971), it is concluded
that in modulation of the LGB synaptic transmission I-cells are the key station not
only for facilitation but also for inhibition.
METHODS
Albino rats, weighing 200-300 g, were used. They were anesthetized with urethane
(1 g/kg of body weight, intraperitoneally)
and placed in a stereotaxic apparatus by the
method of Fifkova and Marsala (1967). One percent procaine was applied to all pressure
points. Thereafter, administration of a small dose of urethane was repeated as required,
so that a constant level of light anesthesia was maintained throughout one experiment.
Under such conditions the pattern of EEGs recorded from the visual cortex was fluctuating
from synchronization to desynchronization at long intervals.
Bipolar electrodes, each consisting of two steel wires insulated except at tips and
separated by about 1 mm, were introduced into the optic tract (OT) at the optic chiasm
and into MID stereotaxically.
An electrode for OT stimulation was positioned at a depth
from which responses to single flash stimulation of the eyes were recorded with high ampli
tudes. An electrode for MID stimulation was fixed usually at AP 2 .0-2.5, ML 0-0.5 and
DV 5.0-5.5. When MID electrodes were positioned with displacements from the midline,
they were on the same side as the target LGB. In some experiments , the placement of
MID electrode was adjusted by observing recruiting responses of the visual cortex to 4-5
Hz repetitive shocks applied through the electrode.
EEG recordings from the visual
cortex were made by a bipolar electrode which was of the same type as applied for stimula
tion of OT and MID and inserted about 1 mm below the cortical surface .
OT stimulation
was made with rectangular
pulses of 0.01-0.05
msec duration
with
intensities
below 50 V. Stimulus
pulses applied to MID were of 0.05-0 .5 msec duration
and their intensities
were comparable
to those for OT stimulation.
Unitary
activities
of LGB were recorded
extracellularly
by means of glass pipette
microelectrodes
filled with 3 M KCl.
A microelectrode
was introduced
into LGB stereo
taxically
and units responding
to single OT shocks were encountered
3 .5-4.5 mm below
the cortical surface.
Unitary
discharges
were amplified,
displayed
on the screen
of a
cathode ray oscillograph
and photographed
on stationary
or running
film .
At the end of some experiments,
a direct current was passed through MID electrodes .
The brains were taken out, fixed in formalin
and embedded
in paraffin . The positions
of
MID electrodes
were examined
histologically
in sections
stained
with
thionine . The
stimulated
sites of the thalamus
were n. paracentralis
, n. centralis
medialis
and a most
mediocaudal
portion of n. medialis dorsalis.
RESULTS
Inhibitory effects of MID stimulation upon P-cells
P-cells respond to single OT shocks with mostly single spikes at late ncies
less than 10 cosec (Burke and Sefton 1966a; Noda and Iwama 1967; Sumitomo
et al. 1969; Fukuda and Iwama 1971; Fukuda 1973). Using Fukuda's termino
logy (1973), this short-latency discharge will be called "initial spike (IS) ." Usually
i
IS
s followed by a silent period of spontaneous discharges which ter minates with
a burst of 2-5 spikes more than 150 cosec later (Burke and Sefton 1966a; Fukuda
Thalamic
Stimulation
and Lateral
Geniculate
Transmission
229
1973). This later occurring burst of spikes will be termed "late discharge (LD)"
(Fukuda 1973). It is often observed that the burst of spikes recurs twice or more
at about the same interval. In terms of membrane potential, the response of
P-cells to OT stimulation may be a short-latency EPSP followed by long-lasting
IPSPs, the former securs spike discharges and each of the latter is terminated by
a depolarizing potential that fires the cell. This has been confirmed in previous
studies with the intracellular recording technique (Fuster et al. 1965; Burke and
Sefton 1966c; Suzuki and Kato 1966; McIlwain and Creutzfeldt 1967; Maekawa
and Rosina 1969; Singer and Creutzfeldt 1970; Kato et al. 1971).
Effects upon IS. First it will bee shown that a single conditioning shock to
MID acts to inhibit ISs of P-cells evoked by testing OT shocks. This is exempli
fied by record of Fig. 1. The control IS, shown in column a, was elicited by OT
shocks with the intensity twice the threshold. Its latency, measured from shock
artefact to the starting point of the diphasic spike, was 3.3 cosec at mean with a
stimulus-to-stimulus variation less than 0.5 msec. In this P-cell a single MID
shock with a fairly strong intensity had no excitatory effect (record f). This was
always true in other P-cells.
Records of columns b, c, d and e were obtained by applying testing OT shocks
which were preceded by conditioning MID shocks at varying time intervals. In
column b where the conditioning-testing interval was 20 msec, the response
probability of IS was reduced definitely and some evoked ISs suffered a slight
prolongation of the latency. The MID-induced inhibition was most potent when
examined at 60 cosec after the conditioning shock (column c). Thereafter the
inhibition lessened gradually, as seen in columns d and e which were obtained with
Fig.
1. Responses
of a P-cell to single OT shocks under effects of conditioning
stimulation
of MID.
a, control.
ISs were evoked at latencies
of about 3.3 msec.
In b, c, d and e single
MID shocks
preceded
testing OT shocks by 30, 50, 100 and 200 msec, respectively.
f, controls for MID shocks alone.
In this and all subsequent
in one column were obtained
by consecutive
sweeps.
figures,
records
presented
230
I. Sumitomo
Fig. 2. Response probabilities of IS in six P-cells (ordinate) as functions of time after
single conditioning stimulation of MID (abscissa). See details in text.
the
conditioning-testing
Effects
stimulation
intervals
of conditioning
were examined
and are illustrated
of 100 and
in Fig.
2, where
the response
the basis of consecutive
ten OT shocks,
conditioning-testing
interval
as abscissae.
evident
around
20 msec
after
msec and wanes gradually
were also found to receive
started
as early
200 msec,
respectively.
MID stimulation
upon responsiveness
of P-cells to OT
in nine units.
The data in six units were fairly uniform
a MID
probabilities
shock,
reaches
the
toward
200-300
msec.
the inhibition
from MID.
as 10 cosec after
of IS, determined
on
are plotted
on ordinates
against
the
It is seen that
inhibition
becomes
a conditioning
maximum
at 50 to
100
The remaining
three units
In one unit the inhibition
MID
shock,
whereas
in the
other
two units
inhibition
it was first detected
at 60-80 msec.
In these three units the maximal
was as strong as in the units shown in Fig. 2 and the recovery from the
inhibition
was
almost
complete
toward
300 msec.
Inhibition of spontaneousdischarges. Most P-cells were discharging sponta
neously at frequencies varying from one cell to another. The inhibitory effect
of MID stimulation was also proved with the spontaneous discharge. A typical
example is shown in Fig. 3. This P-cell was discharging at a frequency of 15/se(
in the control stage (IA). When MID was stimulated at 3.7 Hz, the spontaneous
discharge was almost completelystopped as long as the thalamic stimulation was
continued (IB). Following cessation of the thalamic stimulation the original
level of spontaneous activity was promptly resumed (IC).
Records
this
case
failed
Hz,
to
an
of
OT
evoke
almost
Fig.
shocks
3 ‡U
were
ISs.
complete
Fig.
were
applied
3
IIB
silence
obtained
with
shows
of
the
from
an
the
that
intensity
while
spontaneous
same
so
OT
unit
weak
shocks
discharge
as
that
in
Fig.
they
were
was
3
I.
In
occasionally
applied
brought
at
about,
3.7
Thalamic
Fig.
3.
Effects
of
discharges
A,
control
C,
after
of
induced
may
that
was seen only
discharge
of
Geniculate
MID
(I)
and
Transmission
of
OT
(‡U)
231
upon
spontaneous
B,
was
during
3.7
Hz
stimulation.
Dots
indicate
stimuli.
stimulation.
similar to that
suggested
that
Although
no systematic
the frequency
of MID
neous
stimulation
stimulation.
of
inhibition
and Lateral
P-cell.
before
It was noted
lation
low-frequency
a
cessation
this being quite
is thus strongly
Stimulation
be the
inhibition
when
the
obtained
by low-frequency
the neuronal
mechanism
same
as involved
in the
of the spontaneous
P-cell
stimulus
frequency
was kept
MID stimulation.
It
involved
in the MIDOT-induced
activity
below
a certain
studies were made, it was observed
in many
stimulation
was increased
to some 20 Hz and
enhanced
one.
by MID
stimu
level.
P-cells that
the sponta
definitely.
Observations on LD. LD, a burst of spike discharges occurring more than
150 msec after a single OT shock, is regarded as a rebound excitation following an
inhibition (Burke and Sefton 1966a, b, c; Fukuda 1973). A prolongation of the
latency of LD and/or an increase of the number of spikes contained in LD may
mean that the inhibition preceding LD is longer lasting and more intense.
The following experiment, made by taking LD as an index, revealed that
MID stimulation acted to potentiate or enhance inhibition of P-cells induced by
OT impulses. In the experiment of Fig. 4, a P-cell was fired by OT shocks which
were so weak that ISs were rarely followed by LDs and moreover, elicited LDs
contained only one spike (column A). In column B, weak conditioning shocks
were applied to MID 20 cosec before OT shocks. MID stimulation alone was
232
I. Sumitomo
Fig. 4.
Provocation
of LDs
by combined
stimulation
of OT and MID.
A, control responses of a P-cell to weak OT shocks. Only ISs were evoked unfailingly.
B, same OT shocks as in A were preceded by MID shocks by 20 msec. In A and B
sweeps were started synchronously with OT shocks (dots). C, correlation diagram
between frequency of occurrence of LD (firing probability) (ordinate) and average
number of spikes in evoked LD (abscissa).
Open circles, data by OT shocks alone.
closed circles, data by combined stimuli. Data from same units were joined.
unable to cause any sign of excitation in this P-cell. In response to the combined
stimuli LD appeared more frequently and it contained more spikes than control.
The same experiment was made in other five P-cells and all the data are assembled
in Fig. 4 C as a correlation diagram between the frequency of LD and the average
number of spikes contained, both determined by consecutive ten trails of stimula
tion. Open and closed circles, joined together for each unit, represent the values
determined by OT shocks alone and by the combined stimuli, respectively. In
all cases addition of MID stimulation to OT stimulation was effective in increasing
the frequency of LD and with one exception, the number of spikes contained ,
too.
In the experiment of Fig. 5, OT shocks were intensified so as to elicit LD
unfailingly. The latency of LD in this P-cell was fixed around 280 cosec (Fig .
5A). When this unit was subject to the effect of conditioning MID shocks which
preceded testing OT shocks by 20 msec, the latency of LD was lengthened by
about 60 msec as compared with control (Fig. 5B). The results of the same
experiment from a total of 24 P-cells are summarized in Fig . 5 C. In all the units
tested, the latency of LD was prolonged by combined stimulation of OT and MID .
It ranged from 140 to 325 msec (mean, 213 cosec) for OT stimuli alone and shifted
to the range from 150 to 340 msec (mean, 245 msec) for the combined stimuli .
Post-inhibitory rebound excitation of P-cells following MID stimulation . Now
that MID stimulation has been found to exert an inhibitory effect upon P -cells
which is about the same as produced by OT stimulation , it is expected that the
MID-induced inhibition may be followed by a rebound excitation such as seen as
LD for OT stimulation. There were found some P-cells in which such expectation
was substantially fulfilled. One typical example is shown in Fig . 6B. Although
this cell did not show any sign of primary excitation to MID shocks , spikes were b
urst with a latency of about 230 msec. This burst of spikes is very similar to the
Thalamic
Stimulation
and Lateral
Geniculate
Transmission
233
Fig. 5. Prolongation of latency of LD by conditioning MID stimulation.
A and B were
recorded from the same P-cell. Sweeps were started simultaneously with OT shocks
(dots). A, control responses to OT shocks alone. B, responses to combined stimuli.
MID shocks were applied 20 msec earlier than OT shocks. C, latencies of LDs in 24
P-cells, determined with OT shocks (open circles) and with combined shocks (closed
circles).
Fig. 6. Postinhibitory rebound excitation to stimulation of OT (A) and of MID (B). Sti
muli are indicated by dots. In A ISs were followed by LDs whereas in B only LDs
were elicited.
ordinary LD caused by OT shocks (Fig. 6A).
Records of Fig. 7 were obtained from another P-cell which also showed a
long-latency spike burst to MID stimulation. In this experiment the tip of a
microelectrode was carefully brought to the cell membrane as close as possible in
order to approximate the intracellular recording (quasi-intracellular recording,
McIlwain and Creutzfeldt 1967). In such recordings each of the spike bursts to
MID stimulation was found to be preceded by a negative wave of a long duration.
A similar negative wave was also seen after each of spike discharges occurring
spontaneously (Fig. 7B).
From P-cells of the rat LGB, Burke and Sefton (1966c) recorded extracellularly
a slow negative wave of about 150 msec duration in response to single optic nerve
stimulation. Since such a slow negative wave had the same properties as the field
positive
recorded in the ventrobasal nucleus, Burke and Sefton called it
"P -wave"wave
according to the terminology of Andersen et al . (1964) and interpreted
234
I. Sumitomo
Fig. 7. Quasi-intracellular
recording from a P-cell. A, responses to MID shocks applied
at the start of sweep. Slow negative waves (upward deflections) were followed by
LDs. B, slow negative waves following spontaneous discharges.
Fig. 8. Responses of an I-cell to stimulation of OT (A) and of MID (B). In each column
fast sweeps were used for topmost two records to show initial grouped discharges only.
Other records were made with slow sweep to show a sequence of grouped discharges.
Stimuli are marked by dots.
it as an extracellular sign of the IPSP. Later, Fukuda and Iwania (1971) confirmed Burke and Sefton's finding and supported their interpretation. Since the
slow negative wave of P-cells caused by MID stimulation is essentially the same
as that recorded by Burke and Sefton (1966c) and Fukuda and Iwama (1971) by
using OT stimulation, it seems now safe to conclude that MID stimulation sets
up IPSPs in P-cells and in some cases the latter are terminated with a burst of
spikes as a rebound excitation.
Effects of MID stimulation upon internuncial cells (I-cells)
Burke and Sefton (1966b) were the first who suggested that a long-lasting
inhibition of P-cells following single shock stimulation of the optic pathway might
be the recurrent inhibition mediated via I-cells which were activated by axon
collaterals of P-cells. Although no conclusive evidence has not yet been presented
for or against the existence of the recurrent inhibitory circuit within LGB, the
proposal of these workers that I-cells may be inhibitory neurons acting upon P-
Thalamic
Fig. 9. Provocation
MID.
A, MID
Stimulation
and Lateral
Geniculate
Transmission
235
of initial grouped discharge
by simultaneous
stimulation
of OT and
stimulation.
B, OT stimulation.
C, combined
stimulation.
cells has been supported by other investigators (Suzuki and Kato 1966; Sakakura
1968; Fukuda and Iwama 1971). Since MID stimulation is as effective as OT
stimulation for causing a long-lasting inhibition of P-cells, it is surmised that Icells may play an essential role in the MID-induced inhibition as in the OT-induced
one.
Cells of the rat LGB identified as the I type were those which responded to
single OT shocks with a group of several spikes followed by similar grouped dis
charges recurring at long intervals (Burke and Sefton 1966a; Sumitomo et al.
1969; Fukuda and Iwama 1971). The latency of the I-cell response to OT stimu
lation, measured with respect to the first spike of the earliest grouped discharge
(initial grouped discharge), ranged from 3.0 to 8.0 cosec (Noda and Iwama 1967;
Sumitomo et al. 1969; Fukuda and Iwama 1971).
Primary
MID.
excitation.
A typical
OT shocks
are
shown.
discharges
displayed
discharge
is followed
column
the
I-cells
example
The
with
first
a fast
by the
B one can see that
same pattern
were
is shown
two
sweep.
second
this
as obtained
all
excited
in Fig. 8.
records
I-cell responded
single
in the
The others
one and
by single
by
In column
shock
top
are
show that
sometimes
the
grouped
the initial
grouped
by the third
There
of
to single
initial
to single MID shocks
OT shocks.
stimulation
A the responses
one, too.
In
with virtually
was elicited
the
initial
grouped discharge
followed by the second one with an interval
of more than 200
msec.
In some sweeps more delayed
grouped
discharges
were also seen.
The
latency of the first spike of the initial grouped discharge to MID stmulation
ranged
from
2.1 to 7.9 msec
with
the
mean
of 5.1 msec
in a sample
of ten
I-cells.
In the experiment of Fig. 9 the stimulus intensity of MID stimulation was
slightly below the threshold of the initial grouped discharge (column A) and that
of OT stimulation was just sufficient to evoke only one spike occasionally (column
B). When the two stimuli were delivered simultaneously, this I-cell was strongly
236
I. Sumitomo
Fig.
10. Inhibitory
effect of MID stimulation
upon OT-induced
discharges
of an I-cell.
A, response
to a strong MID shock.
B, control responses
to OT shocks.
In C, D,
E and F subliminal
MID shocks preceded
OT shocks by 40, 60, 100 and 200 msec,
respectively.
Dots indicate
OT shocks.
Fig.
11. Effects of MID stimulation
upon spontaneous
discharges
of an I-cell.
A, control.
In B, C and D frequencies
of MID stimulation
were 0.5, 5.0 and 20 Hz, respectively .
MID shocks are marked
by dots.
excited showing an initial grouped discharge of more than five (column C). These
results indicate that there is a convergence of the excitatory volleys from MID
and OT onto I-cells.
Inhibition following primary excitation. That MID stimulation causes in Icells not only the primary excitation but also the inhibition is shown in Fig . 10.
In the I-cell studied in this experiment, strong MID shocks induced an initial
grouped discharge (record A) which was as vigorous as those produced by OT
shocks (column B). In the series from column C to F , MID shocks were given
as conditioning stimuli with an intensity subliminal for the initial grouped dis
charge and were followed at varying intervals by testing OT shocks which were
of the same intensity as in column B.
In column
responses
C where
were about
the
the conditioning-testing
interval
same as in control.
In column
was 40 msec
D where
, the testing
the two shocks
Thalamic
Stimulation
and Lateral
Geniculate
Transmission
237
were apart by 60 msec, the excitation by OT stimulation was evidently reduced.
Such was more marked for the shock interval of 100 msec (column E). At the
interval of 200 msec there were no significant modifications in the excitatory effect
of OT stimulation (column F). In several I-cells, reduction of the OT-induced
excitation was maximum around 100 msec after the conditioning MID stimulation.
In I-cells showing spontaneous discharges at relatively high rates, the inhibi
tory effect of MID stimulation was clearly evidenced as suppression of the ongoing spontaneous discharges. Sample records are presented in Fig. 11. In the
control stage this I-cell was discharging at a frequency of about 22/sec (column
A). To each of 0.5 Hz MID stimulations the cell showed two or three grouped
discharges spaced by long intervals during which there were no spontaneous
discharges (column B). In column C the frequency of MID stimulation was
increased to 5.0 Hz. While this stimulation was continued, no discharges were
elicited except the initial grouped discharge following each stimulus. Upon increas
ing the stimulus frequency up to 20 Hz, the cell was completely silenced (column
D). This is interpreted that in the steady state of high-frequency stimulation of
MID the inhibition dominated over the excitation so that the cell underwent a
sustained inhibition. The fact that I-cells are continuously inhibited by highfrequency stimulation of MID seems to be closely related to enhancement of
spontaneous discharges of P-cells by continuous stimulation of MID at high
frequencies.
DISCUSSION
With the intracellular technique Purpura and his associates made extensive
studies on responses of cat thalamic neurons to low-frequency stimulation of the
medial thalamus (Purpura and Cohen 1962; Purpura and Shofer 1963; Purpura
et al. 1965, 1966; Maekawa and Purpura 1967). These workers have established
that a majority of the thalamic neurons exhibit a sequence of a short-latency
EPSP followed by a long-latency, prolonged IPSP while the medial thalamic
stimulation is continued at low frequencies. The cell's firing is suppressed during
the IPSP and tends to be confined in the brief period of the EPSP.
The responses of I-cells to low-frequency stimulation of MID are in good
agreement with the observation of Purpura and his associates in the majority
of the thalamic neurons; I-cells are excited at short latencies by each shock of lowfrequency stimulation of MID and this excitation is followed by a long-lasting
inhibition which is terminated by a rebound excitation. In P-cells, however, the
effect of the same thalamic stimulation is different from that seen in I-cells. In
P-cells a single MID shock gives rise to a long-lasting inhibition without being
preceded by an excitation. The fact that P- and I-cells are distinguished in the
response pattern to low-frequency stimulation of MID is taken as a further support for the already established concept that these two groups of LGB cells may
subserve different functions in visual information transfer (Burke and Sefton
1966a, h, c; Fukuda and Iwama 1971; Fukuda 1973).
238
I. Sumitomo
From
are
the
primarily
be made
that
fact
that
inhibited
the
in response
whereas
primary
to low-frequency
I-cells
inhibition
are
primarily
of P-cells
is most
stimulation
excited,
likely
of MID
P-cells
a suggestion
due
to the
may
primary
excitation
of I-cells, i.e., I-cells which are inhibitory
neurons
acting upon P-cells
are excited
by MID shocks and in consequence
P-cells undergo
inhibition.
The
nature
inhibition
as that
MID-induced
is consistent
were
all found
of P-cells
induced
inhibition
with the
induced
by
by OT stimulation.
MID
stimulation
Moreover,
is about
the
it has been shown
same
that
in
the
and the OT-induced
one add up to a stronger
one.
This
finding that I-cells, identified
as such by OT stimulation,
to be activated
by
MID
stimulation.
High-frequency stimulation of MID causes a marked increase of spontaneous
discharges in P-cells. This fact is a thalamic event corresponding to the cortical
one that stimulation of the thalamic non-specific nuclei at low frequencies causes
synchronized EEG responses (recruiting responses) while the same stimulation at
high frequencies results in EEG flattening or desynchronization (Dempsey and
Morison 1942; Morison and Dempsey 1942; Hunter and Jasper 1949; Jasper 1949;
Morruzi and Magoun 1949; Monnier et al. 1960). Purpura and Shofer studied
the synaptic mechanism of this phenomenon at the thalamic level and suggested
that inhibition of inhibition might result in activation of thalamic cells. This
interpretation is found valid for the present findings ; high-frequency stimulation
of MID causes suppression of I-cells, hence P-cells may be released from a tonic
inhibition due to spontaneous discharges of I-cells. This is essentially the same
as the mechanism for facilitation of P-cells by high-frequency stimulation of the
midbrain reticular formation (Fukuda and Iwama 1971).
It has long been recognized that cortical recruiting responses to low-frequency
stimulation of thalamic non-specific nuclei closely resemble EEG waves observed
in one type of sleep called slow wave sleep. Also it has been shown that slow wave
sleep is the state most favorable for the cortex to exhibit recruiting responses
(Yamaguchi et al. 1964). Since P-cells are inhibited when low-frequency stimula
tion is applied to MID and the latter is a member of thalamic non-specific nuclei
(Jasper 1949; Ajmone-Marsane 1965), it is reasonable to suppose that during slow
wave sleep there may be depression of synaptic transmission in LGB . Several
experiments have been published showing that during slow wave sleep synaptic
transmission in LGB is less efficient than during waking (Palestini et al . 1964;
Dagnino et al. 1965; Walsh and Cordeau 1965; Iwama et al . 1966; Kasamatsu and
Iwama 1966). Concerning behaviors of individual cells of LGB during sleep and
waking Sakakura (1968) made an important observation . In freely behaving cats he
found that discharges of P-cells, either spontaneous or evoked by single OT shocks,
decreased when the animal's state shifted from waking to slow wave sleep and in
contrast to this, an enhancement of spontaneous discharges of I-cells was associated
with a developement of slow wave sleep . This fact can be taken as a behavioral
correlate for the present result obtained from acute experiments .
Fukuda and Iwama (1971) have established that suppression of I -cells causes
Thalamic
facilitation
Stimulation
and
of P-cells as a consequence
Lateral
Geniculate
of high-frequency
Transmission
stimulation
239
of the midbrain
reticular formation.
The present experiment has provided evidence that P-cells
are inhibited by low-frequency stimulation of the thalamic non-specific system as
a result of activation of I-cells.
These findings, taken together, clearly indicate
that higher center control
mediation of I-cells.
of synaptic
transmission
in LGB is always executed by
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