Light Scattering Changes Follow Evoked Potentials From
Hippocampal Schaeffer Collateral Stimulation
DAVID M. RECTOR, GINA R. POE, MORTEN P. KRISTENSEN, AND RONALD M. HARPER
Brain Research Institute and Department of Neurobiology, University of California, Los Angeles, California 90095-1761
INTRODUCTION
A number of studies have shown a topographical arrangement of neural activation within the dorsal CA1 region of the
hippocampus (Amaral and Witter 1989), including specific
locations that exhibit activity patterns dependent on the animal’s position within its environment (O’Keefe and Dostrovski 1971). Typically, these studies are performed with
arrays of microelectrodes or multiple placements of one electrode (Rawlins and Green 1977) that contain minimal information about the spatial location of the cell, or with tract
tracing procedures with limited temporal resolution. Optical
procedures provide substantial spatial visualization advantages over electrical measurements for assessing neural activation and offer insights into cellular mechanisms, such as
interactions between large numbers of cells, that are difficult
to examine with microelectrode techniques. Voltage-sensitive dyes have been successfully used to determine the ar-
rangement of cellular activation from a large number of
neurons with the use of imaging procedures. However, these
studies have been limited to reduced preparations (Cohen
1973) or cortical surface structures for short time periods
because of dye toxicity (Arieli et al. 1995).
Changes in light reflectance and scattering, without the
use of dyes, have been used to assess activity in slice preparations (MacVicar and Hochman 1991), cortical structures
in intact animals and humans (Frostig et al. 1990; Grinvald
et al. 1986; Haglund et al. 1992), and subcortical structures
in freely behaving animals (Rector and Harper 1991; Rector
et al. 1993a,b, 1994, 1995). Such optical changes originate
from several slow physiological processes, including transformations in chromophores such as hemoglobin and cytochrome oxidase. Rapid optical changes originate from shifts
in tissue refraction by membrane reconformation and cellular
swelling, which can occur as quickly as voltage changes
(Cohen and Keynes 1971; Landowne 1993).
Early reflectance studies primarily measured light changes
with slow time courses (1–3 s) as a consequence of restrictions in detector sensitivity or data acquisition (Grinvald et
al. 1986). However, light scattering changes can occur as
rapidly as individual action potentials and show two components in rat neurohypophysis activation, a fast membraneprotein-related response that precedes peak voltage change
and a slower ionic exchange response (Salzberg et al. 1985).
Ionic-related swelling also occurs in superposition with action potentials (Tasaki and Byrne 1992). However, studies
of rapid optical changes related to cell swelling, without
the use of dyes, have been previously limited to in vitro
preparations.
To determine whether swelling-related light scattering
changes occur as rapidly and robustly as evoked electrical
responses, and to characterize the topographical patterns of
cellular response in vivo, we assessed the extent of 660-nm
light scattering changes, together with evoked potentials, in
the hippocampal CA1 region following contralateral Schaeffer collateral stimulation. Because the various physiological
processes that contribute to optical changes have characteristic time courses, acquisition of light scattering changes simultaneously with electrical changes at high temporal resolution serves to define the physiological contributions to light
recordings.
METHODS
Six cats were anesthetized with 25 mg/kg pentobarbital sodium
and maintained at a constant anesthesia level with intravenous drip
of 5 ml pentobarbital sodium in 250 ml lactated saline (0.6 ml/
0022-3077/97 $5.00 Copyright q 1997 The American Physiological Society
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Rector, David M., Gina R. Poe, Morten P. Kristensen, and
Ronald M. Harper. Light scattering changes follow evoked potentials from hippocampal Schaeffer collateral stimulation. J. Neurophysiol. 78: 1707–1713, 1997. We assessed relationships of
evoked electrical and light scattering changes from cat dorsal hippocampus following Schaeffer collateral stimulation. Under anesthesia, eight stimulating electrodes were placed in the left hippocampal CA1 field and an optic probe, coupled to a photodiode or
a charge-coupled device camera to detect scattered light changes,
was lowered to the contralateral dorsal hippocampal surface. Light
at 660 { 10 (SE) nm illuminated the tissue through optic fibers
surrounding the optic probe. An attached bipolar electrode recorded
evoked right hippocampal commissural potentials. Electrode recordings and photodiode output were simultaneously acquired at
2.4 kHz during single biphasic pulse stimuli 0.5 ms in duration
with 0.1-Hz intervals. Camera images were digitized at 100 Hz. An
average of 150 responses was calculated for each of six stimulating
current levels. Stimuli elicited a complex population synaptic potential that lasted 100–200 ms depending on stimulus intensity and
electrode position. Light scattering changes peaked 20 ms after
stimuli and occurred simultaneously with population spikes. A
long-lasting light scattering component peaked 100–500 ms after
the stimulus, concurrently with larger population postsynaptic potentials. Optical signals occurred over a time course similar to
that for electrical signals and increased with larger stimulation
amplitude to a maximum, then decreased with further increases in
stimulation current. Camera images revealed a topographic response pattern that paralleled the photodiode measurements and
depended on stimulation electrode position. Light scattering
changes accompanied fast electrical responses, occurred too rapidly
for perfusion, and showed a stimulus intensity relationship not
consistent with glial changes.
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min). A saline-filled catheter measured esophageal pressure for
respiratory assessment. Needles placed in both forelimbs recorded
electrocardiogram. A stereotaxic frame was used to stabilize the
head and to allow accurate electrode placement. A 12 1 7-mm
opening was made in the skull over each hippocampal structure.
The overlying cortex was suctioned and a 2 1 4 array of eight
bipolar stimulating electrodes was lowered to the left dorsal hippocampal surface. The anterior/medial electrode was targeted to coordinates A5.5, L3.25, H10.5 (Berman 1968). Each electrode was
separated by 1 mm. The left opening was subsequently filled with
artificial cerebral spinal fluid, sealed with bone wax, and covered
with dental acrylic.
Figure 1 illustrates the construction of the image probe. The
right dorsal hippocampal structure was illuminated by a 660 { 10
(SE)-nm light-emitting diode (Digikey, Thief River Falls, MN)
FIG . 2. Four successive coronal sections, separated by
1 mm, illustrate placement of 8 stimulating electrodes
(left) and optical probe and electrical recording electrode
(right). Stimulation output to each electrode is controlled
by a 1 of 8 relay selector circuit, which is controlled by
a computer. The computer also stores the CCD camera
output and signals from the polygraph amplifiers for photodiode and electrical measurements, which are digitized
by an A/D converter. Bottom right corner: successive 60mm coronal slices through the hippocampal structure were
scanned into a computer and a dorsal view of the hippocampus was reconstructed. White circles: stimulating electrode placement (E1–E8, left) and photodiode and electrical recording positions (right).
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FIG . 1. Schematic drawing of the optical probe shows a high-sensitivity
photodiode or charge-coupled device (CCD) camera (a) coupled to an
image conduit (b) that is placed on the surface of the hippocampus and
receives scattered light. Illumination light is provided by flexible optic fibers
(c) attached around the image conduit perimeter and transmitting light from
a 660-nm light-emitting diode (d). Concurrent electrical measurements are
made from a wire electrode (e) that extends 0.5 mm beyond the image
surface.
coupled to flexible illuminating fiberoptics (Edmund Scientific,
Barrington, NJ) in contact with the tissue at coordinates A2.5,
L6.25, H10.0. In three cats, a 1.6-mm fiberoptic image conduit
(Schott Fiber Optics, Southbridge, MA), surrounded by illuminating fibers, collected and transmitted scattered light to a photodiode
detector (PIN-HR008, UDT Sensors, Hawthorne, CA). In another
three cats, the image conduit transmitted light to a high-framerate charge-coupled device (CCD) video camera (TC211, Texas
Instruments, Dallas, TX), with a 60-dB signal-to-noise ratio. A
bipolar electrode for recording field potentials was lowered adjacent and anterior to the image probe (A3.5, L6.25, H10.5), and
the opening was filled with artificial cerebral spinal fluid and sealed
with bone wax to minimize movement artifact.
The image probe provided several advantages over conventional
reflectance measurements, including the capability of recording
from structures deep to the cortical surface; dark-field illumination
allowed detection of scattered light changes. Because illuminating
fibers and image conduit were in contact with the tissue, illumination light entered the tissue around the perimeter of the image
conduit and was scattered by the tissue before being captured by
the image conduit for detection by the photodiode and camera. The
capture of scattered light provides minimal light loss over lenscoupled systems. The extent of unaltered reflected light from the
tissue surface (background signal) is minimized, and the diminished background signal allows higher amplifier gain settings. Indeed, in vitro investigations show significantly higher signals under
dark-field illumination over transmission or reflectance mode microscopy (Holthoff et al. 1994).
Stimulating electrode placements on the left side and recording
electrode and optical probes on the right side are shown in four
coronal histological slices in Fig. 2. Each of the eight stimulating
electrodes was separated by 1 mm and targeted for the CA1 region
of the dorsal hippocampus. A serial reconstruction of successive
hippocampal slices shows a dorsal view of electrode and optical
probe placement.
Outputs of the photodiode, field potential recording electrode,
esophageal pressure transducer, and electrocardiogram electrodes
were amplified (Grass Instruments, photodiode and field potential
electrode filter settings 0.1 Hz–3 kHz), written to polygraph paper,
digitized by an A/D converter (AD872, Analog Devices, Norwood, MA, 12 bits, 2.4 kHz), and transferred and stored by a
host computer (Advanced Logic Research, Irvine, CA). The CCD
LIGHT SCATTERING CHANGES FOLLOW EVOKED POTENTIALS
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RESULTS
Figures 3–5 show data from one animal (C3681) to illustrate the electrical and optical responses to stimulation. Other
animals showed similar responses with different regional
FIG . 3. Electrical (thin black line) and optical (thick gray line) responses for stimulating electrode E1 at 100 mA current are plotted over
2,000- and 40-ms time periods around the stimulus (animal C3681). Stimulus artifact (bottom, F ) is followed by an early population spike on the
electrical trace and a corresponding dip in reflectance. Top: longer-latency
electrical postsynaptic potential and corresponding drop in reflectance on
the optical signal. Decreased reflectance corresponds to increased tissue
activation. Vertical lines: SE for each time point from an average of 150
trials.
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FIG . 4. Electrical and optical responses for stimulating electrode position E1 at 6 current levels show a rise in the optical response from 20 to
100 mA stimulating current that declines with further increases in current
(animal C3681). The peak electrical response ceases to increase beyond
200 mA stimulation current and it changes in shape.
effects. Variations in stimulus response across animals may
represent differences in probe or electrode placement or differences in the arrangement of collateral projections between
animals. Stimulation produced a complex population spike,
evoked potential, and afterpotential on the metal electrodes
(Fig. 3). A very fast component of the reflectance response
developed within 5 ms of the stimulus artifact. Stimulating
electrodes produced characteristic responses with each current setting (Fig. 4). The amplitude of the reflectance fast
component (50–200 ms) increased with increasing stimulus
intensity until a level was reached at which further stimulus
intensity increases produced a decrease in the reflectance
response amplitude.
Additionally, each stimulating electrode position elicited
a different level of response (Fig. 5). In the example shown,
stimulating electrodes at positions E1 and E7 produced the
largest response, both electrically and optically, for lowcurrent stimuli. Various components of the optical response
occurred with a time course similar to that of the electrical
response, but in the opposite direction, because there is an
inverse relationship between electrical and scattered light
activity measures. Stimulus potency (i.e., intensity that elicited the peak response in the electrical and optical signal)
is superimposed on the hippocampal dorsal view. The diameters of the white circles in Fig. 5, bottom, show placement
of each stimulating electrode and indicate the effectiveness
of the electrode in producing a peak response. Electrodes
E1 in the top left corner and E7 in the bottom right corner
of the array are represented by the largest circles, because
these placements required the lowest current to produce the
peak response.
A summary of peak and nadir responses across all animals
shows that the peak response of the electrical signal increases
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camera output was scanned by the computer and digitized (12 bits)
such that, within a subregion of the CCD pixels, every other pixel
within each line was skipped and every other line was skipped.
This procedure produced a 100 1 80-pixel image with reduced
resolution but a higher frame rate (100 Hz). The computer also
randomly selected one of eight stimulating electrodes through a
relay control circuit and signaled the stimulator to generate a 0.5ms pulse of six amplitudes: 20, 50, 100, 200, 300, and 400 mA
constant current. Stimuli were delivered every 5 s, and data were
transferred continuously to a mass storage device on the computer.
After the recording, 150 traces from 300 ms before and 2 s after
the stimuli were averaged for each stimulating electrode and current level. Average amplitude and SE for electrical and optical
signals were plotted across time. Images from the CCD camera
were averaged on a pixel-by-pixel basis across time and displayed
as a difference image relative to an average image of 150 sham
stimuli from the same time during the response. Images were pseudocolored such that warm colors (yellow to red) represent increased activation (decreased reflectance) and cool colors (blue to
purple) represent decreased activation (increased reflectance).
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FIG . 6. Summary response levels for all stimulating positions (E1–E8)
at 6 current levels (20–400 mA) across all animals. Reflectance values
have been inverted for comparison with electrical values. Positive traces:
peak values for electrical (black) and optical (gray) signals that diverge at
stimulating current levels ú200 mA. Negative traces: nadir values that are
more correlated for all current levels. Vertical lines: SE of the peak values
at each stimulus current level. Asterisks: significant difference ( P õ 0.05,
Student’s t-test) in normalized electrical and optical peak values.
DISCUSSION
Evoked light scattering changes occurred with fast and
slow time components. The complex nature of the response
indicates that a combination of mechanisms underlies the
optical changes. The peak of the fast response first increased
and then decreased with increasing stimulation current, indicating that inhibitory mechanisms may be recruited at higher
stimulus intensities. Different stimulation sites elicited characteristic response patterns, and sites with peak response
amplitudes suggest a structural connectivity of the Schaeffer
collaterals. The images in Fig. 8 show a stationary pattern
in which components of the image increased and decreased
in amplitude, and the stationary patterns indicate that the
changes may be generated by groups of cells that act in
synchrony rather than in a sequential manner.
FIG . 5. Responses from stimulating electrode E1–E8 at 100 mA stimulus current show that positions E1 and E7 produce the largest response
(animal C3681). Stimulating electrode positions E3 and E4 produce the
smallest responses. Bottom: dorsal view of the cat hippocampus with superimposed stimulating (left) and recording (right) electrode positions. Circle
diameter on the right side: effectiveness of the position for eliciting an
evoked response on the right side. Thus larger circles (E1 and E7) represent
the lowest stimulus currents needed to elicit a maximal response.
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Mechanisms
Multiple time components in the optical response indicate
that several processes may be responsible for light scattering
changes observed within in vivo preparations. Neural activation
elicits a number of optically relevant changes, each with characteristic temporal signatures. Activated neurons demonstrate
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with stimulus intensity to 200-mA stimulating current and
then does not significantly increase with increased current
beyond 300 mA. Optical signals for each stimulating electrode diverge with increasing stimulus intensity ú300 mA.
The nadirs of the electrical and optical late responses are
similar for all stimulus intensities (Fig. 6).
Averaged CCD images in another animal ( C3684, Fig.
7 ) , collected during the peak electrical response, show an
overall response pattern similar to that recorded with the
photodiode but also reveal patches and columns of heightened and depressed activity from the tissue surface. In
this example, peak responses were elicited by electrodes
E2 and E7. Figure 8 illustrates an average temporal sequence of images collected from animal C3763 during
150 trials in which 100-mA stimulation of electrode E7
was used.
LIGHT SCATTERING CHANGES FOLLOW EVOKED POTENTIALS
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modifications in refractive index concurrent with membrane
potential fluctuations that alter light scattering and may contribute to the majority of the rapid changes observed in these
studies (Cohen and Keynes 1971; Roper et al. 1992; Tasaki
and Byrne 1992). Light reflectance is altered by hemoglobin
concentration and oxygenation state changes that show slow
temporal responses to tissue activation (Raichle et al. 1976).
Hemoglobin changes are best observed with green light, however, and may contribute only to the slow response component
(Perkampus 1971). Other slow metabolic trends include cytochrome oxidase conformational changes that alter absorbance
of much shorter wavelength light. Glial cells swell among activated tissue as they absorb excess interstitial ions (MacVicar
and Hochman 1991; Walz and Hinks 1985). The glial response
occurs over seconds to minutes, as opposed to activity of neurons, which shows changes within a millisecond. Axons, dendrites, and smaller interneurons exert greater proportional vol-
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ume change on discharge and may affect reflectance to a greater
extent than larger cells.
Several factors indicate involvement of inhibitory circuits during stimulation. Stimulating collateral pathways that do not lead
directly to the region under the optic probe may elicit inhibition
of the surrounding areas, because images in Fig. 7 show several
stimulating electrode positions that produce a maximal response,
as indicated by the yellow-to-red pixels, and adjacent electrode
positions produce a significant number of blue pixels, or decreased activation. Additionally, stimulus currents ú200 mA
elicit a decreased change in scattered light amplitude, indicating
recruitment of inhibitory mechanisms; this latter finding suggests
a neural rather than glial basis for the changes.
Comparison with electrical measurements
Hippocampal cellular interactions that produce electrical responses in vivo are complex. For example, interactions be-
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FIG . 7. Averaged images from the period of peak evoked response for all stimulating positions (E1–E8) were subtracted
from averaged images collected during
sham stimuli. Difference images show patterns of activation from the dorsal hippocampal surface (animal C3684). Intensity
values are pseudocolored such that yellow
to red represents increased activation (decreased reflectance) and blue to purple represents decreased activation (increased reflectance) with an absolute range of {0.1%
after correcting for camera baseline adjustments.
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tween pyramidal cells and inhibitory interneurons set up a
system of spreading activation and inhibition. Thus, multiple
peaks on the evoked response show a combination of initial
activation and recurrent inhibition and activation from collaterals. Multiple peaks were not observed on light scattering signals. The multiple peaks on the electrical signals may represent
signals detected by electrodes through volume conduction, and
do not have a comparable representation on the optical signal.
The tissue volume through which light scattering changes can
be detected depends largely on illumination wavelength, with
longer wavelengths penetrating through more tissue. For 700nm illumination, detectable light scattering is limited to 500
mm (Malonek et al. 1990), whereas electrically evoked potentials can travel several centimeters through brain tissue and
skull depending on the magnitude of the response. This finding
demonstrates the advantage of light measurement procedures,
which can record the spatial organization of local changes in
neural activity with less contamination by volume conduction
effects from surrounding tissue than is the case with electrical
measurements.
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Schaeffer collateral projection mapping
Multiple stimulation electrode positions provided a course
projection map of Schaeffer collaterals. Two electrode positions, E1 and E7, produced the largest response at low stimulus currents and may be aligned along laminar projection
pathways (Amaral and Witter 1989; Ikeda et al. 1989; Tamamaki and Nojyo 1990). Images collected during the peak
evoked response reveal a topographic arrangement of
patches and columns that differs with each position of the
stimulating electrode. Because our imaged area was relatively small, the images do not show large areas of inactivation and activation in the same frame, as would have been
expected if we had imaged across several functional columns
(Rector et al. 1993b).
Summary
Evoked light scattering changes occur with a time course
similar to that of the evoked electrical response. The rapid
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FIG . 8. Averaged images during 100-mA stimulation of electrode E7 (animal C3763) show a similar pattern of activated
regions from frame to frame, but with underlying variations in amplitude throughout the response. Stimulation occurs during
the frame outlined in red. Frames represent an average of 150 trials at each 10-ms interval before and after stimulation,
subtracted from an average frame at the same time point collected during an equivalent number of sham stimuli. To reduce
the number of displayed images, every 3rd frame is displayed. Pseudocoloring is the same as described for Fig. 7.
LIGHT SCATTERING CHANGES FOLLOW EVOKED POTENTIALS
components were most likely governed by cell conformation
and swelling changes, whereas slow changes may result from
a combination of neural, glial, and blood effects. The results
provide the opportunity to record fast neural events in vivo
that correspond to evoked responses or synchronized slowwave activity.
We thank S. Sampogna and the Brain Research Institute Microscopic
Techniques Laboratory for assistance in preparing the post mortem tissue
for histological analysis. We also thank Xilinx University Program for
donating tools necessary for developing hardware to rapidly digitize camera
images.
This research was supported by National Heart, Lung, and Blood Institute
Grant HL-22418. G. R. Poe was supported by a Howard Hughes Medical
Institute Fellowship.
Address reprint requests to R. M. Harper.
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Received 24 January 1997; accepted in final form 14 May 1997.
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