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1 Department of Psychology, University of Alberta, Edmonton, T6G 2E9 Alberta, Canada; 2 Division of Neuroscience, University of Alberta, Edmonton, T6G 2E9 Alberta, Canada
Submitted 10 August 2002; accepted in final form 9 December 2002
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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). The pretectum
and accessory optic system (AOS) work together to analyze optic flow and
generate the optokinetic response (OKR) to facilitate retinal image
stabilization (Grasse and Cynader
1990; Simpson
1984; Simpson et al.,
1988). Retinal image stabilization ensures optimal visual acuity
(Carpenter 1977;
Westheimer and McKee 1973) and
velocity discrimination (Nakayama
1981).
The AOS and pretectum are highly conserved in vertebrates. The mammalian
pretectal nucleus of the optic tract (NOT) is homologous to the nucleus
lentiformis mesencephali (LM) in birds, whereas the avian nucleus of the basal
optic root (nBOR) of the AOS is homologous to the medial and lateral terminal
nuclei (MTN, LTN) of the mammalian AOS
(Fite 1985;
McKenna and Wallman 1985a;
Simpson 1984;
Simpson et al., 1988;
Weber 1985). AOS and pretectal
neurons have extremely large receptive fields and exhibit direction
selectivity to large-field visual stimuli moving in the contralateral visual
field. Most LM and NOT neurons prefer temporal-to-nasal (T-N) motion (NOT:
Collewijn
1975a,b;
Distler and Hoffmann 1993;
Hoffmann and Distler 1989;
Hoffmann et al., 1988; Hoffman
and Schoppmann 1975, 1981; Ibbotson et
al., 1994; Ilg and Hoffmann
1996; Mustari and Fuchs
1990; Volchan et al.,
1989; Yakushin et al.,
2000; LM: Fan et al.,
1995; Fite et al.,
1989; Katte and Hoffmann
1980; McKenna and Wallman
1985b; Winterson and Brauth
1985; Wylie and Crowder
2000; Wylie and Frost
1996). MTN and LTN neurons prefer upward or downward motion
(Cooper and Magnin 1986;
Grasse and Cynader 1982,
1984;
Natal and Britto 1987;
Soodak and Simpson 1988). nBOR
neurons prefer upward, downward, or nasal-to-temporal (N-T) motion
(Burns and Wallman 1981;
Gioanni et al. 1984;
Morgan and Frost 1981;
Rosenberg and Ariel 1990;
Wylie and Frost 1990).
In response to drifting sine wave gratings, pretectal and AOS neurons
exhibit tuning in the spatio-temporal domain. In the NOT of wallabies,
Ibbotson et al. (1994)
distinguished two groups of neurons: those that preferred high spatial
frequencies (SFs) and low temporal frequencies (TFs) versus those that
preferred low SFs and high TFs. Given that velocity = TF/SF, these two groups
were referred to as "slow" and "fast" neurons,
respectively. Strikingly similar observations were found in the LM
(Wylie and Crowder 2000) and
nBOR of pigeons (Crowder and Wylie
2001).
There is a massive projection from the AOS to the pretectum (mammals:
Baleydier et al., 1990; Blanks
et al., 1982,
1995; Giolli et al.,
1984,
1985a,b,
1992;
Kato et al., 1995;
Mustari et al., 1994; birds:
Azevedo et al., 1983;
Brecha et al., 1980;
Wylie et al., 1997); however,
the physiological significance of this projection has not been studied
extensively (Baldo and Britto
1990; Gu et al.,
2001; Hamassaki et al.,
1988; Nogueira and Britto
1991; Schmidt et al.,
1994,
1998;
van der Togt and Schmidt
1994). In the present study we investigated the contributions of
the nBOR-LM projection to the direction and spatio-temporal tuning of LM
neurons by recording their responses before and after the nBOR was inactivated
by injection of tetrodotoxin (TTX).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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The methods employed conformed to the Guidelines established by the
Canadian Council on Animal Care and were approved by the Biosciences Animal
Welfare and Policy Committee at the University of Alberta. Details for
anesthesia, extracellular recording, stimulus presentation, and data analysis
were previously described by Wylie and Crowder
(2000). Briefly, pigeons were
anesthetized with a ketamine (65 mg/kg)/xylazine (8 mg/kg) mixture (im) and
supplemental doses were administered as necessary. Based on the pigeon
stereotaxic atlas (Karten and Hodos
1967), sufficient bone and dura were removed to expose the brain
and allow access to the nBOR and LM with vertical penetrations. Recordings
were made with tungsten microelectrodes (2–5 M
impedance). The
extracellular signal was amplified, filtered, displayed on an oscilloscope,
and fed to a window discriminator. TTL pulses representing single spikes were
fed to a 1401plus [Cambridge Electronic Designs (CED)] and
peri-stimulus time histograms were constructed with Spike2 software
(CED).
Stimulus presentation
After units in either the nBOR or LM were isolated, the direction preference and the approximate locations of the receptive field boundaries and hot-spot were qualitatively determined by moving a large (90° x 90°) handheld stimulus in various areas of the visual field. Directional tuning and spatio-temporal tuning were determined quantitatively with sine-wave gratings that were generated by a VSGThree graphics computer (Cambridge Research Designs, Cambridge, UK), and back-projected onto a tangent screen that was located 50 cm from the bird (90° x 75°). Direction tuning was tested using gratings of an effective SF and TF at 15° or 22.5° increments, whereas spatio-temporal tuning was tested using gratings of varying SF [0.03–2 cycles per deg (cpd)] and TF [0.03–6 cycles per s (Hz)] moving in the preferred and anti-preferred directions. Each sweep consisted of 4 s of motion in one direction, a 3-s pause, 4 s of motion in the opposite direction, followed by a 3-s pause. Firing rates were averaged over 3–5 sweeps. Contour plots of the mean firing rate in the spatio-temporal domain were made using Sigma Plot.
General procedure
The general procedure was as follows. 1) Locate the nBOR based on
stereotaxic coordinates and extracellular recording, noting the dorsal extent
of the nBOR. 2) Replace the recording electrode with an injection
canula (30 gauge) filled with TTX (Sigma-Aldrich, St. Louis, MO) in
phosphate-buffered saline (pH = 7.4). The canula was positioned such that the
tip was 100 µm above the location of the dorsal-most responsive cell from
the recording track. 3) Lower a recording microelectrode into the
pretectum and characterize the direction and spatio-temporal tuning of an LM
unit (see Stimulus presentation above). 4) Inject TTX into
the nBOR. The time course and maximum diameter of sodium-channel blockade
after an injection of TTX in solution depend on the volume and concentration
of TTX used, and have been shown to approximate that of the diffusion process
from an instantaneous point source
(Zhuravin and Bures 1991). In
some experiments we used a rather large volume of TTX, 1–1.5 µl, but
at a weak concentration of 2 ng/µl. In other experiments we used a more
conservative volume of 0.3–0.5 µl but at a concentration of 10
ng/µl, which is typically used to produce a pharmacological inactivation
(Baldi et al., 1998;
Bielavska and Roldan 1996;
Gallo and Candido 1995;
Rashidy-Pour et al.,
1996a,b;
Roldan and Bures 1994;
Zhuravin and Bures 1991).
[Note that approximately the same absolute amount (2–4 ng) of TTX was
used for both types of injections.] 5) After 15 min, the response
properties of the LM unit were tested again. In some cases, an electrolytic
lesion was placed at the recording site by passing a current of 30 µA for
8–10 s (electrode positive).
Histology
At the end of the recording session, the animals were given an overdose of sodium pentobarbitol (100 mg/kg) and immediately perfused with saline (0.9%) followed by paraformaldehyde [4% in 0.1 M phosphate buffer (PB), 4°C]. Brains were extracted, postfixed for 2–12 h (4% paraformaldehyde, 20% sucrose in 0.1 M PB), and cryoprotected in sucrose overnight (20% in 0.1 M PB). Frozen sections (45 µm thick in the coronal plane) through the LM and nBOR were collected. Sections were mounted onto gelatin chrome aluminum–coated slides and lightly counterstained with neutral red or cresyl violet. The tissue was then examined using light microscopy to confirm the locations of electrode tracks and electrolytic lesions in the LM and the canula tracks in the nBOR.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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After isolating an LM unit, it took approximately 1 h to collect the
pre-TTX data. On subsequent injection of TTX into the nBOR, recording was
maintained for up to 5 h. As the effects of TTX begin to decay after as little
as 2 h (Zhuravin and Bures
1991), we considered only the first 2 h after the TTX injection in
our analyses. The activity of a given neuron before and after the TTX
injection is referred to as "pre-TTX" and "post-TTX,"
respectively.
"Normal" properties of LM units
All 18 LM units were direction selective
(Fig. 3). A unit's direction
preference was assigned by calculating the maximum of the best cosine fit to
the tuning curve. Eleven, 4, 1, and 1 LM units preferred forward (i.e.,
temporal to nasal), downward, backward, and upward motion, respectively
(Fig. 2A,
Table 1). The remaining unit
was a bidirectional neuron, which showed excitation to both forward and
backward motion (see Fig.
3D). The predominance of neurons preferring forward
motion is consistent with previous studies of the pigeon LM
(Gu et al. 2001;
Winterson and Brauth 1985;
Wylie and Crowder 2000;
Wylie and Frost 1996).
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All 18 units were tuned in the spatio-temporal domain. Contour plots were
constructed where TF was on the ordinate, SF was on the abscissa, and firing
rate (relative to the SR) was plotted on the z-axis. Because motion
in the preferred and anti-preferred directions generally results in excitation
and inhibition of the neuronal firing, respectively, we refer to excitatory
and inhibitory response plots (ER plots, IR plots) (e.g., Figs.
4 and
5). Some units showed a single
maximum in the contour plot (e.g., Fig.
4A) but two peaks was more common (e.g., Figs.
4B,
5A–D). Based on
the method of Perrone and Thiele
(2001) the locations of the
peaks in the contour plots were assigned quantitatively by fitting each peak
to a two-dimensional Gaussian function: G'(u, 
) =
{exp[–(u')2/
x2]} x
[–(')2/y2] + P,
where u' = (u – x) cos 
+ ( – y) sin
and ' = –(u – x) sin + ( – y)
cos , and where u is the Ln SF of the test grating, is the Ln
TF of the test grating, is the angle of the Gaussian, (x, y) is the
location of the peak of the Gaussian (in u and coordinates), and
x and y are the spread of the Gaussian in
the u' and ' dimensions, respectively. The G values were
normalized, and added to a constant (P). The values x,
y, x, y, and P were optimized to minimize the sum of the
mean error between the real and G values using the solver function in
Microsoft Excel. In Fig.
2B the locations of the primary peaks from the ER plots
are shown. Consistent with previous studies of the pretectum
(Ibbotson et al., 1994;
Wylie and Crowder 2000), the
peaks cluster into two quadrants: units responding best to gratings of low
SF/high TF (11 cells) or high SF/low TF (7 cells). Following Ibbotson et al.
(1994) we refer to these as
"fast" and "slow" cells, respectively.
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Changes in spontaneous rate of LM units after nBOR inactivation
Table 1 shows the percentage change in the spontaneous rates (SR) of LM units after nBOR inactivation {for decreases, %change = [(post-TTX – pre-TTX)/pre-TTX] x 100; for increases, = [(post-TTX – pre-TTX)/post-TTX] x 100}. For 11 cases there was a significant decrease in SR (15–56%), whereas 2 cases showed a significant increase (7 and 39%) (t-test, P < 0.0028; Bonferroni correction for multiple comparisons), and 5 cases showed no significant change. The average change in SR across all 18 cases was –16.2%.
Effects of nBOR inactivation on the direction tuning of LM units
Figure 3 shows the direction tuning curves for 6 LM units, pre-TTX (solid line) and post-TTX (broken line). Only one unit (Fig. 3F) showed a substantial change in direction preference (116°). For the other units, the direction change did not exceed 12° (mean = 5°) (see Table 1).
From Fig. 3 it is apparent
that the breadth of tuning changed for some LM units. Typically, the
half-power [(maximal excitation – SR)/2] is used to quantify the breadth
of excitation. The half-power bandwidth was determined by measuring the angle
from the origin to the two points where the tuning curve intersected the
half-power value. (This type of analysis was not appropriate for the
bidirectional unit.) For example, the breadth of tuning increased for the unit
in Fig. 3E (43°),
and decreased for the unit in Fig.
3A (–16°). Four units showed an increase in the
half-power bandwidth of 
15° (post-TTX – pre-TTX), whereas 2
units showed a decrease of 15° (see
Table 1).
The magnitude of modulation, both excitation and inhibition, was altered for some units (e.g., Fig. 3B). The %change in the magnitude of excitation and inhibition was calculated from the tuning curves for each unit. Across all 18 cases, there was an average decrease in the magnitude of excitation post-TTX of –17.3%, which was significantly different from zero (single sample t-test, P < 0.02). With respect to the magnitude of inhibition, a more dramatic and consistent pattern was observed. Averaged across 16 cases (i.e., excluding the units in Fig. 3, D and F), the magnitude of inhibition decreased by –36.1%, which was significantly different from zero (single sample t-test, P < 0.002).
Spatio-temporal changes after nBOR inactivation
The spatio-temporal properties were examined pre-TTX for all 18 units, and for all but one unit post-TTX (case #15). The bidirectional cell did not have an IR plot. Thus we obtained pre- and post-TTX ER plots for 17 cells and pre- and post-TTX IR plots for 16 cells. The inactivation of the nBOR affected the spatio-temporal profiles of all LM units tested.
In Fig. 4 data from case #3 are shown. Pre-TTX and post-TTX ER and IR plots are shown in A and B, respectively. In these plots the SR is represented by the solid black fill, and excitation and inhibition are represented by red and green, respectively. The stronger the degree of excitation/inhibition, the progressively brighter and less saturated the red/green fill. Thus the peak excitation and inhibition appear off-white. In addition, "difference" plots are shown. These were calculated by subtracting the pre-TTX plot from the post-TTX plot. On the difference plots, solid black fill indicates no change pre- to post-TTX, blue represents negative values or a lower firing rate post-TTX, and yellow represents positive values or a greater firing rate post-TTX. For the cell shown in Fig. 4, with respect to the ER plots (Fig. 4A), pre-TTX there was a single excitatory peak at 1 cpd/1 Hz. Post-TTX, although unchanged in magnitude, the peak was shifted lower on the TF scale. The difference ER plot had a negative peak in the fast region, reflecting the fact that the unit was less responsive to fast stimuli. Note also the positive peak in the difference ER plot at high SFs and low TFs, indicating that the cell showed an increased excitation to these gratings and corroborating the fact that the peak shifted to lower TFs. With respect to motion in the anti-preferred direction (IR plots, Fig. 4B), pre-TTX this unit had a major inhibitory peak at 1 cpd/0.5 Hz, and very small secondary peak (-5 spikes/s) at 0.03cpd/2 Hz. Post-TTX, the secondary peak remained, but the peak in the slow region was virtually eliminated. In fact, post-TTX the cell was excited in response to high SF stimuli at the lowest TF drifting in the anti-preferred direction (+25 spikes/s). The difference IR plot had a positive peak in the slow region, reflecting the loss of the inhibitory response and the appearance of the excitatory response to high SF/low TF gratings post-TTX.
In Fig. 4C, peri-stimulus time histograms (PSTHs) to three different SF/TF combinations are shown. Three sweeps pre-TTX and 3 sweeps post-TTX are shown, and the approximate time at which the PSTHs were collected relative to the TTX injection is provided. These data indicate the reliability of the effects we observed. To 0.6 cpd/2 Hz gratings (top), the excitation to motion in the preferred direction was clearly reduced post-TTX. To 0.5 cpd/0.13 Hz gratings (middle) there was an increased response to motion in the preferred direction post-TTX, and the inhibition to motion in the anti-preferred direction seen pre-TTX was absent. In fact, post-TTX this unit was excited in response to this grating drifting in the anti-preferred direction. To 0.5 cpd/0.5 Hz gratings (bottom) the excitation to motion in the preferred direction was unchanged post-TTX, but the strong inhibition to motion in the anti-preferred direction was absent.
The directional tuning curves for this case, shown in Fig. 3A, were established with 0.5 cpd/0.5 Hz gratings. Consistent with the data in Fig. 4, there was no change in the magnitude of excitation to motion in the preferred direction post-TTX, but the inhibition to motion in the anti-preferred direction was abolished. Clearly, the change in the depth of modulation pre- to post-TTX observed in the direction tuning curves was dependent on the SF/TF combination used. For case #3, if we had used 0.06 cpd/2 Hz gratings we would have observed a decrease in the magnitude of excitation. Likewise, if we had used 0.5 cpd/0.13 Hz gratings we would have observed an increase in the magnitude of excitation.
Changes in the ER plots after nBOR inactivation
Figure 5, A and B, shows the effects of nBOR inactivation on the ER plots of two other LM units. The unit in Fig. 5A (case #10) showed two excitatory peaks in the pre-TTX ER plot (primary, 1 cpd/2 Hz; secondary, 0.06 cpd/16 Hz). Post-TTX the peak in the fast region was absent, but the peak in the slow region was unaffected. The difference ER plot showed a negative peak in the fast region, and a smaller positive peak to the lowest TFs. The unit in Fig. 5B (case #8) had two excitatory peaks in the fast region pre-TTX (primary, 0.125 cpd/0.5 Hz; secondary, 0.125 cpd/16 Hz). Post-TTX the primary peak is present, although at less than half the size, and the peak at 16 Hz disappeared. In addition, a second peak appeared in the slow region (0.5 cpd/0.5 Hz).
All three examples (Figs. 4A, 5, A and B) are quite similar in that the difference ER plots had negative peaks in the fast region, indicating that LM units showed less excitation to low SF/high TF stimuli moving in the preferred direction post-TTX. This was the most common and dramatic effect that we observed in the ER plots. In column eight of Table 1 the presence of peaks in the difference ER plots for all 17 units tested is noted. Negative fast peaks (–fast) and positive slow peaks (+slow) are shown in bold and italics, respectively. In addition, the magnitude of the peak is indicated as the %change for that SF/TF combination [for –ve peaks, %change = (post-TTX – pre-TTX)/pre-TTX; for +ve peaks, = (post-TTX – pre-TTX)/post-TTX x 100]. Of the 17 units tested, 14 had a negative peak in the fast region of the difference ER plots. For these 14 cells, there were four cases in which an excitatory peak in the fast region of the pre-TTX ER plot was virtually eliminated post-TTX (as in Fig. 5A). The average magnitude of these 14 peaks was –67%. For 7 cells there was a positive peak in the slow region of the difference ER plots (e.g., Fig. 4A) and the average magnitude was +61%.
In Fig. 6A, the ER
plots are averaged across all 17 cells. The responses for each cell were first
normalized, using a common scale for the pre-TTX and post-TTX plots. Despite
the averaging, two excitatory peaks were apparent pre-TTX, reflecting the
spatio-temporal preferences of the fast and slow cells. Post-TTX both peaks
were reduced in size, particularly the fast peak, and at the higher TFs. For
the difference ER plot, based on the pooled variance of the associated with
all points in the plot, values above 0.16 (and below –0.16) are
statistically significant (P < 0.05). [The critical difference
(CD) was calculated as follows:
The difference ER plot had a negative
peak in the fast region, which was largest in magnitude (–0.39) at 0.13
cpd/8 Hz (P < 0.002, single-sample t-test). The positive
peak (0.13) in the region of the highest SFs and lowest TFs was not
significantly different from zero.
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Changes in the IR plots after nBOR inactivation
Figure 5, C and D, shows pre-TTX and post-TTX IR plots for two other LM units. The unit in Fig. 5C showed a large inhibitory peak in the slow region pre-TTX (1 cpd/2 Hz), with a secondary peak in the fast region. Post-TTX the primary peak was eliminated, leaving a peak in the fast region (0.06 cpd/2 Hz). The cell in Fig. 5D also had two inhibitory peaks pre-TTX (primary, 0.06 cpd/8Hz; secondary, 0.5 cpd/2 Hz). Post-TTX, both peaks were reduced in magnitude.
For the 16 cells tested, the most common effect of the TTX injection on the IR plots was a decrease in the amount of inhibition in the slow and/or fast regions post-TTX. This was manifested as positive peaks in the slow and/or fast regions in the difference IR plots. The effect on the slow region was more consistent and more dramatic. In 3 cases an inhibitory peak in the slow region was eliminated post-TTX (as in Fig. 4B). Of the 16 difference IR plots, 10 (63%) had positive peaks in the slow region (as in Figs. 4B, 5C) with an average magnitude of –78%. Seven difference IR plots had positive peaks in the fast region with an average magnitude of –60%.
The averaged normalized IR plots are shown in Fig. 6B. Note that post-TTX there is a reduction in the magnitude of inhibition to gratings throughout much of the spatio-temporal domain, although it is particularly dramatic to the high SF/low TF gratings. For the difference IR plot, values above 0.17 (and below –0.17) are statistically significant (P < 0.05). The difference plot had a large positive peak (0.5) in the slow region at 0.5 cpd/0.5 Hz (P < 0.0004, single-sample t-test).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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; Baleydier et al.,
1990; Blanks et al.,
1982,
1995;
Brecha et al., 1980; Giolli et
al., 1984,
1985a,
1992;
Kato et al., 1995;
Mustari et al., 1994;
Schmidt et al., 1998;
Wylie et al., 1997) by
observing the directional and spatio-temporal tuning of LM units before and
after inactivation of the nBOR with TTX. We found that, although the effects
on the directional tuning were minor, the spatio-temporal properties of all LM
units changed after nBOR inactivation. Changes in the directional tuning of LM neurons after nBOR inactivation
In the present study we found that the direction preference of LM units was
rarely altered post-TTX. In some cases the breadth of the tuning was altered,
as was the depth of modulation. Gu et al.
(2001) examined the
directional tuning of LM neurons before and after the nBOR was temporarily
inactivated by lidocaine. However, they used moving bars as stimuli, which are
not as appropriate as large-field stimuli
(Frost 1985). Nonetheless,
with respect to the directional tuning of LM neurons, the results of the
present study are in agreement with those of Gu et al.
(2001). They found that the
inactivation of the nBOR altered the breadth and depth of tuning, but not the
direction preferences of LM neurons. Gu et al.
(2001) used extremely small
volumes of lidocaine and it is unlikely that there was any spread outside the
nBOR. Given that we had similar observations with respect to directional
tuning of LM neurons, we are confident that our observations are not
attributable to the possibility that the TTX spread beyond the nBOR.
Changes in spatio-temporal preferences of LM neurons after nBOR inactivation
This study is the first to demonstrate that the spatio-temporal properties
of LM neurons are affected by the activity of other nuclei in the optokinetic
system. That pretectal neurons are tuned in the spatio-temporal domain was
first shown in the wallaby NOT (Ibbotson
et al., 1994; Ibbotson and
Price 2001). Two groups of neurons were found: "fast"
neurons preferred low SF/high TF gratings, whereas "slow" neurons
preferred high SF/low TF gratings. Subsequently we found such fast and slow
neurons in the pigeon LM and the nBOR
(Wylie and Crowder 2000;
Crowder and Wylie 2001). In
the present study we found that nBOR inactivation changed the spatio-temporal
tuning of LM units. With respect to stimuli drifting in the preferred
direction, after nBOR inactivation, most LM units showed less excitation to
low SF/high TF (i.e., fast) gratings and some units showed more excitation to
high SF/low TF (i.e., slow) gratings. With respect to stimuli drifting in the
anti-preferred direction, after nBOR inactivation, most LM units showed less
inhibition to slow and/or fast stimuli.
Implications for AOS–pretectal connectivity
Data from the present study offer several insights to the nature of the
connection from the nBOR to LM. First, because LM neurons are directional
after nBOR inactivation, it is apparent that other inputs contribute to the
direction selectivity of LM neurons. This is not surprising, given that the LM
receives a direct retinal input (Gamlin
and Cohen 1988a). Using intracellular recording, Kogo et al.
(1998) demonstrated that retinal inputs into the turtle AOS are direction
selective. This is likely the case for the avian AOS and pretectum as well.
The pretectum also receives input from the telencephalon in many species
(Hoffmann et al. 1991;
Hollander et al. 1979;
Schoppmann 1981;
Ilg and Hoffmann 1993;
Lui et al. 1994;
Mustari et al. 1994;
Shintani et al. 1999)
including pigeons (Miceli et al.,
1979), and the lateral cerebellar nucleus in pigeons
(Arends and Zeigler 1991).
Clearly, the visual response properties of LM neurons arise from the
interaction of many inputs. Second, because most LM neurons showed very little
change in their preferred directions after nBOR inactivation, it appears that
the LM receives inputs from nBOR neurons with a similar preferred axis. Thus,
nBOR neurons preferring horizontal motion (forward and back cells) project to
LM neurons preferring horizontal motion, and nBOR neurons preferring vertical
motion (up and down cells) project to LM neurons preferring vertical motion.
Finally, it appears that information from nBOR to LM is specific in the
spatio-temporal domain for stimuli drifting in the preferred and
anti-preferred directions.
The most parsimonious explanation for our results would be that the LM
receives excitatory input from fast nBOR cells of the same direction
preference and/or inhibitory input from slow nBOR cells of the opposite
direction preference. In Fig. 7
we consider the input to the most common type of LM neurons, those that are
excited by forward motion and inhibited by backward motion (i.e., a forward LM
neuron). Figure 7, top
and bottom, shows directional and spatio-temporal tuning,
respectively, for two nBOR neurons (from
Crowder and Wylie 2001). The
ER plots, direction tuning curve, and IR plots are shown for a nBOR neuron
that preferred backward (N-T) motion (top) and a nBOR neuron that
preferred forward (T-N) motion (bottom). The back neuron was
maximally excited by slow gratings (high SFs, mid TFs) and maximally inhibited
by fast gratings (mid SFs, high TFs) drifting forward. The forward neuron was
maximally excited by fast gratings (low SFs, mid-high TFs) and maximally
inhibited by slow gratings (high SFs, low TFs) drifting backward. To account
for our observations of the effects of nBOR inactivation on the responses of
LM neurons, we propose that a forward LM cell receives inhibitory input from
the slow back cell, and/or excitatory input from the fast forward cell.
Although our study does not address which of these two scenarios is more
likely, for a few reasons we favor the inhibitory projection. First, back
cells are much more common than forward cells in the nBOR
(Gioanni et al., 1984;
Rosenberg and Ariel 1990;
Wylie and Frost 1990). Second,
slow cells are more common than fast cells in the nBOR
(Crowder and Wylie 2001).
Finally, previous studies involving electrical stimulation of the AOS have
shown that the projection to the pretectum is largely inhibitory. This has
been shown both in rats (van der Togt and
Schmidt 1994) and pigeons
(Baldo and Britto 1990).
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It is important to note that the proposed model is descriptive and does not
address the reciprocal connection between the nBOR and LM
(Brecha et al., 1980;
Gamlin and Cohen 1988b). Thus
in addition to preventing retina-to-nBOR information from reaching the LM,
nBOR inactivation may also interfere with bidirectional dynamic interactions
between the two nuclei.
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DISCLOSURES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests: D.R.W. Wylie, Department of Psychology, University of Alberta, Edmonton, T6G 2E9, Alberta, Canada (E-mail: dwylle{at}ualberta.ca).
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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