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Biol.

Cybernetics 33, 63 75 (1979) Biological


Cybernetics
9 by Springer-Verlag 1979

Entrainment of Oscillatory Neural Activity


in the Cat's Lateral Geniculate Nucleus*
Conrad Wall, III**, Wlodzimierz M. Kozak, and Arthur C. Sanderson
Biomedical Engineering Program and Electrical Engineering Department, Carnegie-Mellon University, Pittsburgh, Pa., USA

Abstract. Oscillatory neural activity in the frequency The present study is an attempt to characterize the
range 7-12Hz is observed in the lateral geniculate thalamic oscillatory activity observed in the lateral
nucleus (LGN) of the lightly anesthetized cat. This geniculate nucleus (LGN) of the cat. The approach
paper describes a series of experiments in which the taken is based on engineering systems theory and
interactions between ongoing oscillatory potentials regards the LGN as a system with primary input from
and periodic photic and electrical stimuli are analyzed the retina and a measurable output signal in the form
using frequency domain techniques. The principal of a gross neural potential (see Fig. 1). This description
results of these experiments are consistent with a is clearly a simplification as recent physiological evi-
model of the neural system as an entrainable oscillator dence (Singer, 1977) has shown. However, it provides a
in which ongoing oscillations are suppressed by stimu- basis for expressing quantitative relationships describ-
lation at nearby frequencies, but coexist with stimulus ing retinal input and its influence on ongoing intrinsic
frequencies farther away. The physiological interpre- LGN activity. The intent of the work is not to model
tation of these results may be closely tied to the role of the physiological origins of LGN activity in detail, but
the LGN as a "gating" mechanism between retina and rather to derive a description of the interaction be-
cortex. tween the activity and retinal input. Systems theoreti-
cal models provide a useful description of this type of
interaction.

RECORDING
Introduction ELECTRODES

Early studies of electroencephalographic (EEG) ac- OT LGN A


tivity revealed the occurrence of stereotyped oscil-
latory potentials in both surface and intracortical
recordings. Such distinctive wavelike patterns amid an
otherwise noisy signal aroused curiosity about both PHOTIC
STIMULUS~
the physiological origin and the behavioral correlates
of this neural activity. One direction which the study of OT LGN B
oscillatory alpha activity (7-12Hz) has taken is the ELECTRIC STIMULUS;
identification of a similar type of oscillatory com-
ponent in gross electrode recordings from the thalamic
nuclei in mammals. These studies and an argument
which suggests that the alpha activity originates in the
thalamus have been elaborated by Andersen and SEVERED ON
Andersson (1968). Fig. 1. Schematic diagram of experiments. A Diffuse photic stimu-
lation to the contralateral eye with ipsilateral eye in dark or excised.
* Supported by NIH Training Grant 4t:GM01455 and NSF Coaxial recording electrodes in ipsilateral optic tract (OT) and in
Grant # ENG-7515736 layer A of the lateral geniculate nucleus (LGN). B Stimulation using
** Present address: Department of Otolaryngology, University of bipolar electrodes to the contralateral optic nerve (ON) after
Pittsburgh, School of Medicine, Pittsburgh, PA. 15260, USA bilateral enucleation. Recording electrodes as above

0340-1200/79/0033/0063/$02.60
64

In this paper we consider the effect of externally cell and interneuronal responses in the rat during
applied single-pulse and periodic stimuli upon the electric stimulation of the optic tract and visual cortex.
intrinsic, alpha-like, rhythmic activity of the cat's lateral They concluded that the LGN has recurrent inhibition
geniculate nucleus (LGN) that is centered at an expe- capable of oscillating at about 10 Hz. This result has
rimentally measured frequency, f,. This experimental also been discussed by Creutzfeldt (1966), Andersen
approach has led us to examine in detail a class of and Sears (1964), Andersen and Andersson (1968),
engineering models which seem to offer insight into Eccles (1969). More recent studies summarized by
interactions between intrinsic and extrinsic oscillatory Singer (1977) suggest that localized inhibition may be
mechanisms. One of these, the entrainable non-linear mediated by LGN interneurons while more diffuse
oscillator (Pavlidis, 1973), has been examined in the recurrent inhibition may be due to perigeniculate
context of other biological systems, for example, to neurons. These results have suggested that perigen-
model diurnal biorhythms which may be affected by iculate neurons may be associated with the widespread
imposed light-dark programs. We have experimentally oscillatory phenomena.
examined two effects in the LGN which would help to LGN single unit activity was categorized by Levick
differentiate between a linear system model and a non- and Williams (1964) as "stable" or "unstable". Bishop
linear entrainable oscillator model. These are: sup- et al. (1964) divided the unstable units into 2 groups:
pression of alpha-like activity by periodic stimuli, and "fast cyclic" and "rhythmic burst" types. The single
the dependence of the transfer characteristic upon unit stable mean rate and fast cyclic types of firing have
stimulus amplitude. This paper describes these effects their activity drastically changed when the retinal
and relates them to the entrainable oscillator input to the LGN is stopped, but rhythmic bursting
hypothesis. types of activity continue even after the LGN is
isolated from retinal input.
Although the LGN activity investigated in these
experiments is assumed to be intrinsic to the thalamus,
Background inputs from other parts of the brain may influence it.
Important inputs originate from the ascending re-
Previous physiological experiments suggest that there ticular activating system (ARAS) (Arden and
are at least two classes of spontaneous oscillations S6derberg, 1961; Ogawa, 1963; Satinsky, 1968;
which can be observed in the mammalian lateral Bowsher, 1970; Singer, 1973; Singer and Schmielau,
geniculate nucleus (LGN). One of these seems to 1976) and from the pons (Ponto-Geniculo-Occipital,
depend upon light-induced retinal activity (Kozak, PGO, Waves : Singer and Bedworth, 1974 ; Malcolm et
1971) whereas the other appears to be an intrinsic al., 1970; Bizzi and Brooks, 1963). Singer (1977) has
LGN oscillation due to the neural net of the LGN and recently reviewed corticofugal and reticular influences
its associated nuclei and does not seem to require on thalamic structures.
retinal input as a necessary condition for oscillatory Despite the influence of extrinsic factors, the work
behavior. The purpose of our experiments was to of Kato (1974) on the isolated, sliced LGN of the cat
determine what effect externally applied stimuli have provides evidence in support of an oscillatory process
upon the latter, intrinsic LGN oscillation, and to test that is intrinsic to the LGN and is due to the structure
the hypothesis that the LGN is an oscillating system of the neural net. Removal of visual cortices did not
that can be entrained by external periodic signals of stop the oscillation of neurons in the LGN in experi-
appropriate frequency and strength. ments of Satinsky (1968), and he also concluded that
Spontaneous neuronal activity is a feature of most the oscillatory activity may be due to reverberating
sensory systems (Thompson, 1967, p. 287). Oscillatory circuits within the LGN itself.
potentials in the visual system were first observed in Several previous determinations of the LGN tem-
the dark-adapted electroretinogram (ERG) and in the poral transfer characteristics have been made: Maffei
electric records from the optic tract (OT) by Granit and Rizzolatti (1966), using sine-modulated light in
(1933) and by Bartley and Bishop (1942). The response Nembutal-anesthetized cats; Lopes da Silva et al.
to single light flashes in human ERG's (Cobb and (1970a, b) using sine-modulated light in alert dogs
Morton, 1953) also had oscillatory components. having chronically implanted electrodes, and Rosen
Bishop and Davis (1960) showed that the LGN of the and Vastola (1973) who used sine modulation of rapid
cat generated slow (about 10 Hz) rhythms. electric shocks applied to the optic nerve to determine
The discovery of LGN principal cell repetitive the phase shift through the LGN. None of these
firing by Bishop et al. (1953) led them to postulate an experiments, however, were designed to investigate the
inhibitory interneuron associated with the LGN. interaction of the periodic stimulus with the intrinsic
Burke and Sefton (1966a, b, c) recorded single principal LGN oscillations.
65

Methods differentially to battery-powered preamplifiers having


a gain of approximately 1000 and common mode
Experimental rejection ratio (CMRR) of 110 db. In order to prevent
Gross electrode recordings were taken from the optic electromagnetic interference, the preamplifiers and the
tract (OT) and lateral geniculate nucleus (LGN) of cat were placed in a double walled, sheet-steel shielded
fourteen cats, each weighing 2 to 3 kg. An initial dose room (Filtron-Filshield Corp.). The cat's physiological
of 0.6 g/kg Urethan anesthesia (25 % Urethan in physi- body temperature was maintained by a direct current
ological saline) was administered intraperitoneaily. driven heated pad, using feedback control from a
About six hours later, the initial dose was followed thermistor implanted in the animal. Pupils were dilated
by a continuous intravenous infusion of Urethan by instilling Atropine Sulphate ophthalmic solution.
0.05g/kg/hr. Urethan was used because it does not Retraction of the eyelids and maximal pupillary di-
diminish either the fast oscillatory components of the lation were achieved by instilling Neosynephrine 1%
light evoked response (Kozak, 1971), or the intrinsic rhinal solution into the conjuntival sac.
LGN activity. When necessary, small I.V. doses of Light stimuli (Fig. 1A) were delivered either from a
Nembutal were given before the insertion of ear plugs Grass model PS-2 Xenon flash unit which produced
and Novocaine was instilled into the skin incisions. brief (10 las peak width) flashes, or by a direct current
The cat's head was rigidly held in a Horsley- Tungsten light projector (Color Temp. 2800 ~ with
Clarke type stereotaxic apparatus (La Pr6cision electromechanical shutter having an opening time of
Cin6matographique) modified so as not to obstruct the 2 ms and shutting time of 5 ms. The shutter could also
visual field. Holes were drilled in the skull above the be driven by a signal generator to produce a sine-
OT and LGN, and the exposed Dura Mater was modulated light stimulus. Both light sources were
removed. These holes were then plugged with a soft outside the shielded room. The stimulus light passed
wax prosthesis (Lukens 900 bone wax) to prevent through the room walls via a 6 f t x 1/4in. type
cerebrospinal fluid leakage and brain pulsation ULGM-5 fiber optics cable (American Optical) and
(Bishop et al., 1962). Coaxial electrodes (Rhodes shone either directly into the eye or into a concave
Medical Instruments), 0.5mm outside diameter, isol- screen that was in the visual field 75 cm from the eye.
ated outside except for the edge of the outer barrel and Thus, all sources of alternating current electromag-
the tip of the inner wire, were passed through the wax netic noise were effectively isolated from the experi-
into the brain. Such an electrode can discriminate mental animal. The screen luminance for the incandes-
between local and remote generators of electrical cent light projected diffusely on the screen was approx-
activity in a volume conductor by recording differen- imately 15cd/m 2. The Xenon flash intensity of 106
tially between outer barrel and inner wire. lumens was attenuated approximately 6 db by the fiber
Both electrodes were placed on the side con- optics cable. When the Xenon flash was used, the end
tralateral to the eye being stimulated. The OT elec- of the fiber optics bundle was placed approximately
trode tip was placed just posterior to the optic chiasma 1 cm from the cat's eye so the flash shone directly into
at approximate Horsley-Clarke coordinates A+12, the eye. The light intensity could be varied by placing
L + 4 , H - 5 . The L G N electrode tip was placed in neutral density filters over the end of the fiber optics
layer A at approximately A + 5, L + 9, H + 4. Correct cable.
placement of the electrode in the L G N was verified by In three cats, the L G N "input" from the retina was
the visually evoked response with a large peak-to-peak isolated by bilateral eyeball removal (enucleation,
amplitude in one locality indicating local activity. The Fig. 1B). In these cats, the recording electrodes were
placement was also verified anatomically in some cats positioned for a maximum response to light as de-
by removing the cortex and observing the electrode scribed above. Next, the conjunctiva and eye muscles
located in the LGN. The "swish" multi-unit response were dissected away from the eyeball. The optic nerve
(Bishop et al., 1962), driven photically from the con- was exposed using blunt dissection and was ligated
tralateral eye was also used as an indication of correct near the eyeball. Finally, all of the eye was cut away
electrode position. Polarity reversal of the response as from the optic nerve, leaving only a small piece of
the electrode passed through the optic radiation to the retina at the optic disk. This procedure produced a
L G N was also noted (Bishop and McLeod, 1954). temporary injury discharge, which slowly subsided and
High amplitude (100-600gV) simultaneous OT and left very little activity in the OT.
L G N responses were obtained by varying the position The optic nerves of enucleated cats were stimulated
of the stimulus in the visual field until the maximum with electric shocks using a Grass model P S I U 6 B
response was obtained from the OT electrode. Next, optically coupled stimulus isolation unit (SIU) placed
the L G N electrode position was adjusted to give a in the shielded room but connected to the Grass S 88
maximum response. The electrodes were connected stimulator outside it. The SIU output went to a
66

stainless steel bipolar electrode. The electrode was variance in the noise spectral estimate, thus allowing
designed so that the exposed optic nerve could be the harmonic signal to stand out. Spectral averaging
pulled through it after enucleation. The electrode leads also permits one to determine the statistical signific-
were shielded, and the shielding was attached to a ance of spectral peaks. Our approach was to calculate
grounding electrode in the form of a stainless steel a mean and standard deviation of each spectral point
spiral wire wrapping the optic nerve between the point using period averaging of 10-20 repeated trials.
of stimulation and the brain. This minimized the shock
artifact as recorded in the brain.
Results
The overall electrical noise, recorded from coaxial
electrodes in Ringer's solution or from electrodes in Ambient LGN Activity
dead cats, was 5-10 gV peak-to-peak (filter band pass 1
Low frequency ambient activity in the LGN
to 300 Hz) for single sweeps and correspondingly less
(0.5-30 Hz) is characterized by a diffuse band of low
for averaged records (typically 2 laV for an average of
frequency noise in the 0.5 to 3 Hz region and by a
ten sweeps), Spectral analysis of the noise showed no
relatively sharper band of activity centered between 7
significant peaks at 60 Hz and its harmonics, or at any
and 12Hz, depending upon the individual cat. The
other frequencies.
latter activity will be referred to as LGN intrinsic or
The amplitude of the waveforms recorded during
natural oscillation. The amplitude, spectral width, and
the stimulation was from 100 to 600 gV, and therefore,
center frequency of the LGN natural oscillation vary
was well above the abient noise level. Locally made
with time in a single cat. There are periods when the
amplifiers with variable bandpass filters were used to
activity is quite regular. Quiet periods can occur under
amplify the signal and to filter out higher frequency
the effect of barbiturate anesthesia or when there has
signal components that could cause aliasing during
been no stimulus for one half to one hour. This effect
sampling. At this point in the signal processing, the
may be due to a change in the level of the cat's
stimulus signal plus the OT and LGN responses were
alertness or to a reduction of the on-going retinal
recorded using an Ampex model SP 300, AM-FM type
activity. During an active period the oscillation tends
recorder. On-line frequency analysis or multichannel
to occur in wave packets or spindles. The most re-
time averaging was done on a Digital Equipment
gularly occurring spindles are about one second in
Corp. PDP-8/L computer equipped with a multiplexed
duration and recur, on the average, every 2-4 s. Much
10 bit analog-to-digital converter, a 1 KHz clock, and a
of the time the spindles are less regular, both in their
digital-to-analog converter for display purposes. A
duration and in the interspindle intervals.
Grass Model S 88 stimulator controlled timing of the
Figure 2 shows an example of irregular LGN
stimulus and of the start of computer data acquisition.
oscillatory activity. The time record, Fig. 2A, is similar
Analytical to a sine wave to which noise has been added. The
Frequency analysis was performed using the Fast obvious periodicity corresponds to approximately
Fourier Transform (FFT) algorithm (Cooley and 10 Hz, and the peak-to-peak (p-p) amplitude varies
Tukey, 1965) combined with other subprograms to from 20 to 120 ktV. The accompanying averaged ASD
digitize and display data, and then to average and plot plot, Fig. 2B, was obtained from ten segments of
amplitude spectra. Normally, 256 data points were sampled time data, each lasting 2.048 s. The interval
between consecutive sampling sections was ten se-
taken at a sampling rate of 125 Hz (8 ms/address). The
sampled data were multiplied by a raised cosine (han- conds, so that the total time during which the activity
ning) window. The windowed time series was the input was monitored amounted to slightly over two minutes.
For this time the bandwidth of the oscillation shown
data to the FFT algorithm. The result was a discrete
Fourier transform consisting of 128 complex points in on the plot was one Hz and the center frequency was at
the frequency domain. A discrete estimate of the 9.8 Hz.
Although the amplitude of the LGN oscillation is
Amplitude Spectral Density (ASD) was obtained by
taking the square root of the sum of the squares of the time-varying, the frequency of the peak amplitude
never varied more than _+1 Hz for any individual cat
real and imaginary points for each frequency incre-
with intact eyes. Larger changes were recorded when
ment of the FFT output. For convenience, these
the LGN was isolated from retinal activity after
discrete periodograms will be referred to as ASD data.
A specific number of successive ASD data files obtain- enucleation.
ed under the same experimental conditions were aver-
LGN Oscillations Following Bilateral Enucleation
aged together. The averaging procedure is desirable
when there is a harmonic signal superimposed upon a Because the principal afferent connections to the LGN
band-limited white noise, 'because it decreases the are from the retinal ganglion cells via the optic nerve,
67

A
there is a possibility that the 7-10Hz oscillation as
recorded in the LGN could actually originate in the
retina. Simultaneous gross electrode data from 14 cats
showed no evidence of this. There were, however, some
peaks in OT spectra falling in the 2-5 Hz range that
were mirrored in the LGN spectra.
In three cats, the eyes were removed bilaterally to
identify the role of the retinal input on the LGN gross
potential activity. The enucleation reduced the amount
B of low frequency (0.5-20 Hz) activity recorded from the
0. OT electrode, and also decreased the LGN amplitude
O. "~ ( Peokof oscillotion spectral density in the same frequency region, except
for the 7-9 Hz intrinsic oscillations which continued
~,~o. Bood .idth o, following bilateral enucleation. This procedure re-
o
duced other low frequency activity and made the
intrinsic oscillation more obvious. One cat showed a
large increase in the amplitude and regularity of the
LGN oscillations. This is illustrated in Fig. 3. The
"~ 0
typical reduction of the low frequency activity in both
I I
E 10 20 OT and LGN is apparent, along with the increase in
,ci
Frequency in Hz the amplitude of the LGN oscillations. The second
harmonic of the LGN oscillation becomes visible in
Fig. 2. A Intrinsic oscillatory activity in the cat's Lateral Geniculate
Nucleus (LGN). Darkness, eyes intact. A single sweep of ongoing the spectrum taken after enucleation. A slight dimi-
activity. Coaxial electrode. Amplifier band-pass 1-200Hz. B nution (from 8.8 to 7.3 Hz) of the center frequency also
Amplitude spectral density (ASD) of activity shown in A. Bandpass occurs.
1-30 Hz. Ten sweeps averaged in frequency domain. Sampling rate : Table 1 gives the frequency shifts for all three cats
125 Hz. Time series length: 2.048 s. The frequency peak of intrinsic
oscillation of the alpha-type is indicated by arrow after enucleation.
These shifts are equal to, or slightly greater than,
the frequency variability in the LGN oscillations of
cats which were not enucleated.
Table 1. LGN oscillation center frequency

Cat ~ Before After Difference


LGN Response to Diffuse Light of Variable Duration
29 8.3 5.4 -2.9 Hz and to Brief Electric Shocks
30 8.3 6.3 - 2.0 Hz
A b r i e f (50 m s ) f l a s h o f diffuse i n c a n d e s c e n t l i g h t t o t h e
31 8.8 7.3 - 1.5 Hz
c o n t r a l a t e r a l eye p r o d u c e s t h e O T a n d L G N r e s p o n s e

2o] A B

,olFL LoN
,.,or.
Fig. 3A-D. Simultaneous OT and LGN am-
plitude spectral densities (ASD's) before and
o
0
o lo 0 I0 after bilateral enucleation. Different prepara-
0 tion than in Fig. 2. Ten sweeps averaged for
each plot. Sampling frequency 125 Hz. Sweep
2O D
1~ OT Before OT After
lengths 2.048s, as in Fig. 2B. A and C.
Before enucleation, darkness. The alpha-like
! LGN intrinsic oscillation is indicated by the
arrow. Oscillatory activity at this frequency is
IO L___LL,~NoiseLevel absent from the OT record. B and D. Same

~o o
,

10
ot
0 10
,
preparation, after bilateral enucleation. The
oscillatory LGN activity is more coherent,
has a higher amplitude and its second har-
Frequency in Hz Frequency in Hz monic is visible
68

A range is not of retinal origin. Up to this point, however,


Optic there is no indication that the L G N electrode is not
Tract ~,r"~'-:--" -1 IO0
J,u.Volts "picking up" an oscillatory signal from some other
Stim -]-[-- ~ 0.2 Sec
part of the brain, or that "ringing response" is not
simply the superposition of the fast rising peak with an
B independent ongoing oscillation. Figures 4C and D
50
help to clarify these points. A series of six consecutive
LGN l/,c Volts responses to single flashes is shown. The interval
between stimulus presentations varied from 5 to 10 s
and the light source was triggered manually by the
C experimeter. The oscilloscope sweep was delayed
Optic ~ ~.~
]so 100ms after the stimulus to eliminate the first large
Tract "~.. , _ S _ . "~ -- - - ' ~ ' - - " ~ /,c Vo#ts deflection. The repeatability of the L G N response 300
t~l O. I Sec to 600 ms after the stimulus strongly indicates that at
D least part of the L G N ringing response after a single
]50 stimulus pulse is phase-locked to the stimulus and
L GN /z Volts therefore not due to other sources. Note that there is
no evidence of this response in the a T , (Fig. 4C).
Figure 4E gives further evidence that the "ringing"
t ~ l 0.2 Sec E response is due to the stimulus. The oscilloscope sweep
trace was triggered 450 ms before the presentation of
/~ Volts single light pulses so that the L G N activity prior to the
_ _ ~ _ _ stim stimulus could be compared to the activity afterwards.
The after-response is clearly not due to an alpha
Fig. 4. A and B. Electrical responses in the aT and LGN to single spindle that occurred prior to the stimulus.
50ms flashes of diffuse light. Eyes intact. Coaxial electrodes. The L G N ringing response will be larger if the
Amplifiers'band-pass 1-200Hz. An oscillation of about 7 Hz starts
in the LGN 300ms after the flash. There is no similar oscillation in stimulus pulse is given right before or during the
the aT. C and D. Stimulus as above, but different preparation. Six occurrence of a spindle, as opposed to a stimulus given
consecutive superimposed electrical responses to 50 ms diffuse light during a more quiet period. This variability of the
flashes. Sweeps delayed 100 ms after flash onset. Alpha-like oscil- L G N ringing response and its relationship to the
lation at about 10 Hz is visible in the LGN record (D) only. Note
intrinsic spindling activity was not quantitatively in-
that the phase of the oscillations is relativelyconsistent with respect
to the stimulus time. E. LGN response to the single diffuse light vestigated. An interesting related phenomenon was a
pulse delivered to contralateral eye. Sweep is triggered 0.45 s before tendency in some cats for L G N intrinsic spindling to
presentation of pulse be induced by periodic stimulus trains.
The L G N response to a 10 gs light pulse was not
substantially different from a 50 ms one. A short (1 ms)
shown in Figs. 4A and B. There is a fast-rising peak in electric shock stimulus to the optic nerve after bilateral
both the a T and LGN. The L G N response is delayed enucleation did produce and L G N response that dif-
by about 2ms from the a T one. For the cats in- fered from the photic response. This might be expected
vestigated, the peak amplitude of the L G N pulse since all of the afferent excitation reaches the L G N
ranged from 100 to. 600gV, averaging 250txV. In within a period of 1-2 ms, a much more synchronous
addition to the fast rising peak, the L G N response input than can be achieved using photic stimuli. The
exhibits a low frequency oscillation in the 7 to 11 Hz convergence of excitation presumably synchronizes the
range. The onset of this low frequency activity is response of a larger number of L G N cells so that the
typically about 0.5 s following the stimulus. The actual events in the gross L G N response are more closely
center frequency varies from cat to cat. This oscillatory related to the events that occur in the single unit
response tends to die out or decrease in amplitude with response.
time. In this sense, it is like a "ringing" response. The
broad-band filters used in the recording and process-
L G N Response to Periodic Stimulation
ing of the data exhibited no such response. This L G N
ringing response is at approximately the same fre- Periodic stimulation had a somewhat different effect
quency as that of the L G N intrinsic oscillations re- on the L G N oscillations than single pulses. The per-
corded under conditions of no stimulation. iodic light stimulus was 100% modulated either by
The results from the previous section have demon- square waves or sine waves. The peak intensity was
strated that the L G N natural oscillation in the 7-12 Hz equal to that of the single flashes. Stimulus frequency
69

was the significant factor. If the stimulus frequency, fs,


v
was near the frequency of the n a t u r a l oscillation, f,,
_~ 2O then the n a t u r a l oscillation was suppressed. A t sti-
mulus frequencies sufficiently greater t h a n f,, the na-
.c,~
10 tural oscillation r e a p p e a r e d at an a m p l i t u d e a p p r o x i -
m a t e l y equal to t h a t of the oscillatory activity in
6. darkness. The n a t u r a l oscillation also grew stronger
E
< 0 I d u r i n g the p e r i o d s of d a r k n e s s between successive
I0 2O stimulus trains.
Frequency in Hz A p a i r of a m p l i t u d e spectra which illustrate this
s u p p r e s s i o n effect are shown in Fig. 5. The b o t t o m
s p e c t r u m shows the L G N activity between successive
stimulus trains. There is a large p e a k at 8.8 Hz, the
L G N n a t u r a l oscillation. In the t o p spectrum, t a k e n
fn d u r i n g 12 H z flicker, there is no p e a k at 8.8 H z ; there
1

~. 20 is only a p e a k at fs. A l t h o u g h flicker stimulus also


After
r e d u c e d the lower frequency spectral c o m p o n e n t s in
the 0.5 to 3.5 H z range, the latter r e d u c t i o n was n o t as
o
O
10 great as the suppression at f,.
T h e values of the a m p l i t u d e spectra at f~ a n d fs,
t o g e t h e r with their s t a n d a r d errors, are used to show
a.
E
0
20 the suppression effect in Fig. 6. The figures show the
0 10
B Frequency in Hz a m p l i t u d e of the L G N natural oscillation t a k e n at
frequency f . d u r i n g s t e a d y state c o n d i t i o n s (darkness
or s t e a d y light) and d u r i n g p e r i o d i c p h o t i c stimu-
Fig. 5A and B. Amplitude Spectral Densities (ASD's) of the electrical lation. T h e a m p l i t u d e at f , is p l o t t e d vs. the stimulus
LGN activity during and after periodic photic stimulation (Flicker) frequency, f~. A t the right side of the plot is the
at a frequency different from the intrinsic one. Coaxial electrodes.
a m p l i t u d e d u r i n g steady state conditions. T h e fre-
Amplifier band-pass 1-30Hz. Ten responses averaged. Sampling
rate: 125 Hz. Time series length: 2.048 s. Flicker train repetition quency at which the L G N n a t u r a l oscillation occurs is
rate: once every 12s. A analysis of the last 2.048s of the LGN also m a r k e d on the abscissa as f,. The figures show
responses to a 5s flicker train of square 12 Hz flashes. The spectral t h a t the n a t u r a l oscillation is s u p p r e s s e d d u r i n g flicker
peak corresponding to the stimulus frequency stands clearly out. B when the flicker frequency is n e a r the n a t u r a l fre-
As above, but the 2.048 s time series analysed starts six seconds after
the end of the flicker train, f, : frequency of the natural (intrinsic) quency. This suppression effect does n o t c o n t i n u e as
LGN oscillation. This oscillation was absent from the upper record, the stimulus frequency is increased, a l t h o u g h the aver-
so that the system was fully entrained there age level of i l l u m i n a t i o n is the same at all times. Thus,

fn = 9Hz __~ t fn = 9.5 Hz


Fig. 6. Average amplitude of the LGN intrin-
r=2.1 sic oscillations (at frequency f,) during per-
p___<.05 p<.05
iodic photic stimulation at frequencies fs dif-
ferent from f,. The intrinsic component
_ _

amplitude at f, is plotted as a function of fs.


c 18 !
i C 19 Data from four cats, # 18, 19, 20, and 22.
Vertical bars correspond in their length to
, '1, I I 'l, ,
lO 20 S:L. Dark +1 Standard Error (S.E.). Ten responses
10 2O
were averaged for each frequency of stimu-
fn 7.5 Hz fn = 9 Hz lation. Stimulus frequencies f~ which were
remote from f. were less effective in suppress-
r=3.7 } ing the intrinsic oscillations, than the f~ which

,]i'
p < .01 differed only slightly from f~. r: ratio of the
p= .02 difference between the means at neighboring
points to the standard error of the difference
'tJ C 20 C22 of the means, p: t-test significance level, S.L. -
steady light. Coaxial electrodes. Amplifiers'
I I band-pass : 1-30 Hz. Sampling rate : 125 Hz ;
IO 2'0 30 Dark 10 2O 3O 256 points sampled
70

c 20
Oj ,
A and p are shown between the last point that we
interpret as "suppressed" and the first "recovered" one.
All five cats analyzed in this way showed a significant
jump that differentiated the "suppressed" response
-8 from the "recovered" one. This "jump" occurred be-
= I0
tween 15 and 25Hz. We do not have quantitative
0 . . . . information on the influence of the stimulus strength
upon the suppression effect.
fFi B

L G N Frequency Response
The averaged amplitude spectra of simultaneously

~
<
zo
O , , ~
J
,
recorded L G N and O T responses to periodic stimulus
trains of various frequencies were compared. The
spectra were averaged over 10 to 20 successive trials.

,o],CTRANSF
9 R
The stimulus frequency runs were presented in random
fn C order. In some cats, the stimulus strength was varied
by using neutral density filters for photic stimulus and
by varying the stimulus voltage for electric stimulus.
The raw d a t a for each stimulus frequency, f~, consisted
:~0.5 of two averaged amplitude spectra, one for the L G N
and one for the OT. The mean values and the standard
<
deviations of the spectra of f~ were used for the
o frequency response determinations.
0 5 I'0 1'5 io In order to derive a frequency response estimate for
F r e q u e n c y in Hz
the L G N , we divided the L G N frequency response
Fig. 7. A and B LGN and OT tuning curves with electric stimulation function by the corresponding O T frequency response
for one experimental run. Amplitude of spectral peak correspond- function, for each case separately. Figure 7 shows an
ing to the stimulus frequency is plotted versus stimulus frequency. example of the L G N frequency response, the O T
Brackets show _+1 S.E. C Transfer characteristic is derived from OT frequency respons e and the calculated transfer charac-
and LGN. Arrows mark the frequency of the natural oscillation,
f,, which was measured prior to periodic stimulus tests
teristic, for one experiment using electric shock stimuli
to OT. The standard error of the mean of each data
point is marked by brackets and was determined from
the L G N and OT frequency responses. Standard
the L G N natural oscillation recovers when the sti- errors are found using an approximation for the ex-
mulus frequency is sufficiently high. pected value of the ratio of two random variables.
Figure 6 shows that this recovery takes place above
15 Hz. Since all the points on the plot have standard
errors, the significance of the increase in the amplitude
of the L G N natural oscillation above flicker frequen- where :
cies of 15 Hz, can be tested by taking the ratio, r, of the E x = standard error of the transfer characteristic
difference of the mean values divided by the standard E 1 = standard error of the L G N response
error of the difference of the means: E o = standard error of the O T response
A t = L G N response mean value at fs
x-y
r = (sX2 +sp2)i/2 A 0 = the O T response mean value at f~.
This error expression is an upper bound, since it
where: neglects a co-variance term which would reduce the
2 = mean value of the first recovered point error .if the input and output were correlated.
= mean value of the last suppressed point A total of 17 frequency response runs were made in
s2 = standard error of 2 nine cats. Runs for three stimulus intensities were
sp = standard error of y. made in four of these cats. D a t a from six of the nine
F r o m r the probability, p, that this difference would be cats show an absolute or relative m a x i m u m in the
exceeded by chance can then be determined from L G N frequency response, when the stimulus fre-
tables of the t distribution. On each part of Fig. 6, the r quency, fs, is at or near the L G N natural frequency, f,.
71

The transfer characteristics from five of these six cats


also show a corresponding peak. In the other cases, the
transfer characteristics either show peaks at f, which
are not significant at the p < 0.05 level, peaks which are I -
not at f,, or show a constant or decreasing response
with increasing stimulus frequency.
The monotonically rising trends in the OT electric
response data of Fig. 7A can be explained in terms of
I..iJ
the variable duty cycle obtained using a constant
:)
electric pulse width while varying pulse frequency. I-
._1 ! I
In summary, there is good indication of a peak, at (1.
O I 2
the L G N natural frequency, in many individual cat ~E

L G N frequency responses. The individual transfer a


ILl
characteristics also show significant peaks at s but N
not as satisfactorily. The main factors which make the .._1

transfer characteristic questionable seem to come from ~E


n.-
the O T signal. The calculation of ensemble transfer O 2--
z
characteristics, Fig. 8, for both photically and electri-
cally stimulated cats indicates a peak at or near the
L G N frequency of natural oscillation. This peak is I -
more pronounced in the electrically stimulated cats.
Ensemble averaging was carried out as follows:
1) All data were separated according to type of
0 ! !
stimulus, photic or electric. O I 2
2) The frequency axis of each individual tuning
NORMALIZED FREQUENCY ( f * )
curve was normalized to the L G N background oscil-
lation frequency for the individual cat. Fig. 8. A Ensemble transfer characteristics from all photically
stimulated cats. All points normalized to LGN natural frequency.
3) The data were scaled to the means and then Mean and one standard error limits are plotted. Averagedpoints are
averaged to obtain ensemble OT and L G N curves for fitted by a third order spline curve.B Ensembletransfer characteris-
each type of stimulus. tic data from all electricalstimulation experiments
4) Ensemble frequency responses were calculated
for each stimulus type by dividing the L G N response
by the O T response. Instead, the phase leads the input for f~ < f , . The phase
passes through zero when s The phase lags the
input for fs>f,. Figure 9A shows an example for one
L G N Phase Measurements experiment. There are some noticeable deviations from
straight line fits through the data in the region around
Photic Stimulation. Three phase differences were calcu-
f~ = f,, but they are not systematic from cat to cat nor
lated from the experimental data using periodic stimu-
do they shift systematically in one cat when they
lation: the phase shift from stimulus to O T response
stimulus strength is varied.
(O - S) ; the phase shift from stimulus to L G N response
( L - S ) ; and the phase shift from OT to L G N ( L - O ) . Electric Stimulation. Data from the L G N response to
The latter would represent the phase shift through the electric contralateral optic nerve stimulation were used
LGN. In the photically stimulated cats, all three phase to determine the L G N phase difference ( L - S ) in one
shift parameters show a phase decrease with increasing cat. Figure 9B shows the L G N phase difference for
frequency. The phase differences ( L - S ) and ( O - S ) three stimulus intensities. Except for the points within
show a tendency to change slope depending upon the + 1 Hz of the L G N natural oscillation f,, all three
stimulus intensity, but a linear fit of the phase shift phase response curves are nearly the same. In the 3 to
from O T to L G N ( L - O ) does not change slope with 12 Hz region, the curves somewhat resemble those of
changing stimulus intensity. The change of slope with the photically stimulated cats. They show a steady
intensity might imply a change in delay time [-i.e. a phase decrease that goes through zero at or near f,.
transport delay], which in this case would be 23.4 ms However, in the region above 12 Hz, the phase tends to
for photic stimulation. However, the phase parameter flatten out and then to increase slightly. The stimulus
( L - O ) cannot be attributed entirely to a time delay, intensity seems to affect the phase response at stimulus
since the phase does not extrapolate to zero at f, = 0. frequencies near f,. Data from the weakest stimulus,
72

A recorded in the LGN principal cells by Creutzfeldt

1
0.2
(1966) and Singer et al. (1972). The spontaneous ac-
0. I
tivity, Fig. 2A also agrees in frequency with the results
0 /
-0.1
s ,5 io of Bishop and Davis (1960). Spectral analysis of the
0.2 activity, Fig. 2B, is like that found by Lopes da Silva et
0.3 al., (1970a, b) in the dog LGN, except that the fre-
quency of the ongoing oscillation in the dog is about
+0.5
12Hz instead of 7-10Hz in the cat.
"-'Z~ 9 40 Volt Stimulus Most of the experimental frequency response find-
+0.25 \ 0 t 0 Volt Stimulus B ings are similar to those of Maffei and Rizzolatti
\ V 7 Volt Stimulus (1966), who determined the L G N transfer characteris-
0 9 i tics using single unit electrodes. Their gain vs fre-
5 ',~" ' ' OH quency curves agree roughly with ours in that the
response tends to fall off above 10 Hz. Our findings
-0.2 5 in x
show a peak which occurs at the natural oscillation
frequency. The region in which this peak occurs is
-0.5 rather narrow and, unless the test frequency incre-
Fig. 9A and B. Phase transfer points taken from Fourier transform of
ments are equal to 1 Hz or less, it is not likely that the
the time-averaged stimulus, LGN response and OT response. 2.048 s peak would be found. Maffei and Rizzolatti's test
samples taken from the middle of a 3 s long train of square wave frequencies in this region were at 2, 5, and 10 Hz. Their
photic flicker data sampled at 250Hz. Analog filters set 0-30Hz. frequency increments were too widely spaced to have
Stimulus frequency range is from 5-20Hz. A Phase shift (L-O)
resolved the peak response which our data show.
through the LGN taken from a photically stimulated cat. B LGN
phase shift for an electrically stimulated cat. Three different stimulus The phase of our transfer characteristics changes in
voltages are used: 40, 10, ? V the same amount over approximately the same fre-
quency interval as the phase response which Mallei
and Rizzolatti (1966) show. Both the phase changes
amount to approximately - 180 degrees. However, our
7 V, tend to keep the phase shift nearly constant over a data show a phase lead below the natural frequency
3Hz range. Increasing the stimulus strength to 10V and a phase lag when the stimulus is above the natural
decreases this range of "flatness" to 2 Hz. There is no frequency. The data of Maffei and Rizzolatti (1966)
evidence of "flatness" around f, in data from the 40 V show a phase which is always less than or equal to zero
stimulus run. The rate of phase change of a linear fit to degrees, i.e., there is no phase lead in their data. It is
the data in the 3 to 10Hz range gives a slope of possible that the dynamic population response obtain-
approximately -0.15 radians per Hz. If the shift were ed with a gross electrode may differ from the responses
caused by a time delay, the delay would amount the of a single unit.
approximately 75 ms. Rosen and Vastola (1973) also investigated the
To summarize, L G N data from both electrically transfer properties of the lateral geniculate nucleus
and photically stimulated cats show a phase decrease using sinusoidally modulated pulse trains of electric
with increased stimulus frequency. There is a relative shocks applied as a stimulus to the optic tract. It is not
lead below f, and a relative lag above f~. The LGN possible to compare their results with ours directly
phase passes through zero in the region where fs =f,. because they show the relationship between the modu-
For photic stimulation, zero phase occurs at a fre- lation frequencies of the stimuli and the average firing
quency 1-2 Hz higher than f~. The phase shift cannot rates of single cells in the LGN. This averaging
be adequately characterized as a simple time delay. technique measures only the shift in mean firing rate
due to sinusoidal modulation. Such a response is quite
different from the mean transfer functions which are
Discussion discussed here.
The power spectrum of LGN activity recorded by
Comparison of Results with Previous Findings Lopes da Silva et al. (1970a) shows a peak at l l . 7 H z
The pulse response in Fig. 4 with the oscillatory after- which corresponds to the alpha rhythm of the dog
effect is similar to the slow rhythms found in the cat (Lopes da Silva et al., 1973a, b). This spectrum looks
L G N by Bishop and Davis (1960). There is a single quite similar to the spectrum of the spontaneous
spike followed by several cycles of an 8-10 Hz damped activity which we show for cat, Fig. 2B, except that the
oscillation. The period of these oscillations corres- frequency peak for cat is, on the average, somewhat
ponds in frequency to the 100ms postsynaptic IPSP's below 10 Hz.
73

Systems Models shift depends to some extent upon the kind of stimulus.
The strength of the electric shock train stimulus in
While it is difficult to model a complex neural network
some experiments does affect the phase response,
in sufficient detail to interpret the observed behavior in
particularly when the stimulus frequency is close to the
terms of specific physiological phenomena, it is often
L G N natural frequency.
fruitful to explore analogous behavior in order to gai n
The experimental results concerning all the above
insight into a physiological system. Among physical
three points may be related to certain classes of
systems, a particular class of nonlinear system, the
models. The gain results are like those of a second-
entrainable oscillator, would seem to offer such an
order damped linear system, but the results could also
analogy for the present study.
be consistent with the response of a non-linear system
Engineering systems theory treats frequency en-
with small gain dependence upon the stimulus ampli-
trainment in the context of a well-defined self-
tude. The phase results are similar to those of a non-
oscillating system with a fundamental frequency, f,.
linear system because the phase is dependent upon the
Such a system can be mathematically described by a
stimulus strength. In some non-linear systems the
nonlinear differential equation. The mathematical be-
change in phase with stimulus strength is a more
havior of the model is examined using a periodic
sensitive parameter than is the change in gain.
forcing function. Frequency entrainment is said to
A variety of models can be invoked to explain
occur when the driving signal "takes over control of
experimental results. As complexity increases, more
the oscillation frequency" (Cunningham, 1958, p. 213)
results are explained. A single non-linear entrainable
i.e., the component at f, is suppressed or abolished
oscillator model explains our results more completely
during periodic driving by signals of appropriate fre-
than a single linear system model. As a further step, an
quency and sufficient strength. This effect depends
ensemble of non-linear entrainable oscillators might be
upon the strength and frequency of the injected signal
considered.
and upon the characteristic of the nonlinear system
itself.
The following principal characteristics of the ex-
perimental system with periodic stimuli may be com- Conclusions
pared to the entrainment model: The intrinsic oscillatory activity of the L G N suggests
1) Background activity. There is an ongoing neural that large numbers of neurons may "spontaneously"
activity in the L G N and which can be characterized as synchronize. The origin of this synchrony is not clear.
having a frequency component of fairly narrow band- It is reasonable from physiological considerations
width (Fig. 2). The "ringing" response to single light (Singer, 1977) to suppose that such oscillatory activity
pulses (Fig. 4D) strongly suggests that there is an originates within the thalamic structures but may be
interaction between an external visual stimulus and the strongly influenced by other inputs. Recurrent in-
background activity as recorded in the LGN. hibitory feedback exists between the perigeniculate
2) Suppression by Periodic Stimulation. As discussed nucleus and the LGN principal cells, and the mapping
above, frequency entrainment is an effect which occurs of this inhibitory influence in the L G N appears to be
in a system that can be described by a non-linear widespread rather than local. Reticular formation
differential equation that allows a periodic system inputs, in turn, appear to inhibit perigeniculate neu-
"output" to appear even when there is no system rons (Singer, 1977). In addition, recurrent inhibitory
"input". This intrinsic output can be suppressed or interneurons occur within the LGN, though their effect
completely eliminated by certain periodic input sig- seems to be more local. Thus, from anatomical con-
nals. Periodic electrical stimulation to the OT sup- siderations, there appears to be a network of neural
presses the intrinsic, alpha-like, oscillation which oc- interactions which could produce oscillatory activity
curs in the LGN. due to feedback inhibition with a delay resulting from
3) Gain and phase response during periodic stimu- synaptic summation.
lation. The L G N transfer characteristics show a maxi- The control of inhibitory feedback by reticular
mum or relative maximum when the stimulus fre- formation inputs suggests a mechanism which could
quency is at the L G N intrinsic oscillatory frequency. induce or suppress such oscillatory actNity. In this
There is no significant change in the transfer character- case, oscillations would tend to occur when the re-
istic with change in stimulus strength. The phase shift ticular formation is least active or in states of low
of the fundamental frequency through the L G N de- alertness. Behavioral manifestation of the occurrence
creases with increasing frequency, and has a shift of of alpha activity in EEG also suggests that such
zero when the stimulus frequency is at or near the oscillatory activity may be associated with a "resting"
L G N natural frequency, s The nature of the phase rather than "active" state of the neural system.
74

The retinal input to the LGN converges primarily References


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