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1 Department of Psychology, University of Alberta, Edmonton, Alberta T6G 2E9, Canada 2 Centre for Neuroscience, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
Submitted 6 August 2003; accepted in final form 20 September 2003
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ABSTRACT |
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INTRODUCTION |
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; Grasse and Cynader 1990; Simpson 1984; Simpson et al. 1988). The OKR facilitates retinal image stabilization, which is important for optimal visual acuity (Carpenter 1977; Westheimer and McKee 1973) and velocity discrimination (Nakayama 1981).
The AOS and pretectum are highly conserved in vertebrates. The medial and lateral terminal nuclei (MTN, LTN) of the mammalian AOS are homologous to the avian nucleus of the basal optic root (nBOR), and the pretectal nucleus of the optic tract (NOT) in mammals is homologous to the nucleus lentiformis mesencephali (LM) in birds (Fite 1985; McKenna and Wallman 1985a; Simpson 1984; Simpson et al. 1988; Weber 1985). AOS and pretectal neurons have large receptive fields in the contralateral visual field and exhibit direction selectivity to drifting large-field visual stimuli. Most neurons in the LM and NOT prefer temporal-to-nasal (T-N) motion (NOT: Collewijn 1975a,b; Distler and Hoffmann 1993; Hoffmann and Distler 1989; Hoffmann and Schoppmann 1975, 1981; Hoffmann et al. 1988; 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). In mammals, AOS neurons prefer upward or downward motion (e.g., Grasse and Cynader 1982, 1984; Simpson et al. 1979; Soodak and Simpson 1988), whereas nBOR neurons prefer upward, downward, or nasal-to-temporal motion (Burns and Wallman 1981; Gioanni et al. 1984; Morgan and Frost 1981; Rosenberg and Ariel 1990; Wylie and Frost 1990). When drifting sine-wave gratings are used as visual stimuli, neurons in the pretectum and AOS exhibit tuning in the spatiotemporal domain, preferring either high spatial frequencies (SFs) and low temporal frequencies (TFs), or low SFs and high TFs. Because velocity = TF/SF, these 2 groups were referred to as "slow" and "fast" neurons, respectively (Crowder and Wylie 2001; Crowder et al. 2003,Crowder et al. 2003; Ibbotson and Price 2001; Ibbotson et al. 1994; Wylie and Crowder 2000).
Both the AOS and pretectum receive massive retinal input (Mammals: Garey and Powell 1968; Giolli and Guthrie 1969; Hayhow et al. 1960; Scalia and Arango 1979; Birds: Fite et al. 1981; Gamlin and Cohen 1988a; Karten et al. 1977; Reiner et al. 1979). However, the AOS and pretectum also receive numerous extraretinal inputs that could influence the visual response properties of neurons within these nuclei. For example, there is a heavy reciprocal connection between the AOS and pretectum (Rats: Blanks et al. 1982; Terasawa et al. 1979; Rabbits: Giolli et al. 1984; Holstege and Collewijn 1982; Cats: Berson and Graybiel 1980; Itoh 1977; Weber and Harting 1980; Pigeons: Brecha et al. 1980; Clarke 1977; Gamlin and Cohen 1988b; Wylie et al. 1997). Furthermore, the AOS and pretectum receive input from the telencephalon, although this input is quite variable between species. In cats and monkeys, the cortical input to NOT is quite heavy (Hoffmann et al. 1991; Ilg and Hoffmann 1993; Mustari et al. 1994; Schoppmann 1981), but is absent in other frontal-eyed species such as the opossum (Pereira et al. 2000). Moreover, the NOT receives cortical input in rabbits (Hollander et al. 1979), guinea pigs (Lui et al. 1994), and rats (Shintani et al. 1999), but not in hamsters (Lent 1982) or tree shrews (Huerta et al. 1985). In pigeons, both the nBOR and LM receive afferents from the Wulst (Miceli et al. 1979; Rio et al. 1983), which is thought to be the avian homolog of primary visual cortex (Karten and Shimizu 1989; Medina and Reiner 2000).
In the present study we used electrical stimulation and reversible pharmacological inactivation of the Wulst to ask the following questions about the LM. Is the Wulst projection to LM excitatory or inhibitory? Do both fast and slow LM cells receive input from the Wulst? Is the connection correlated with direction preference? Finally with the Wulst inactivation, we sought to determine whether the afferents from the Wulst contribute to the directional and spatiotemporal tuning of LM neurons.
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METHODS |
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The methods used conformed to the guidelines established by the Canadian Council on Animal Care and were approved by the Biological Sciences 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 (intramuscularly), 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 LM, nBOR, and Wulst with vertical penetrations. Recordings were made with glass micropipettes filled with 2 M NaCl and Pontamine sky blue (tip diameters 4–5 microns). 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 peristimulus time histograms (PSTHs) were constructed with Spike2 software (CED).
Visual stimulus presentation
After neurons in the 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 and spatiotemporal 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 22.5° increments. Direction preference was quantitatively assigned by calculating the peak of the best-fit cosine to the tuning curve. Spatiotemporal tuning was tested using gratings of varying SF [0.03–2 cycles per degree (cpd)] and TF [0.03–16 cycles per second (Hz)] moving in the preferred and antipreferred 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.
Orthodromic stimulation
Neurons in the LM received orthodromic electrical stimulation with single shocks (0.5 ms, 25–400 µA, 0.3 Hz) that were delivered through a Teflon-coated stainless-steel bipolar stimulating electrode positioned in the area of the Wulst that contains LM-projecting neurons (12.5 mm anterior and 1.5 mm lateral from interaural zero, 1.5 mm ventral to the surface of the telencephalon; see following text, Technical considerations). The tips of the bipolar electrode were staggered by 0.5 mm. The constant-current pulses were produced by an S48 stimulator (Grass-Telefactor, West Warwick, RI) connected to a PSIU6 stimulus isolation unit (Grass-Telefactor). Note that the 0.5-ms single-shock pulse duration introduces a small measurement error (i.e., about 0.5 ms) because it is difficult to separate response latency from the pulse onset versus pulse offset.
Wulst inactivation general procedure
The procedure to measure the effects of Wulst inactivation was as follows. 1) Based on stereotaxic coordinates, bone and dura overlaying the Wulst were removed, and the bipolar stimulating electrode and injecting pipette [about 25 µm tip diameter, filled with 4% lidocaine (Sigma-Aldrich, St. Louis, MO) in phosphate-buffered saline (pH = 7.4)] were positioned in the Wulst. The stimulating electrode was angled at 45° in the coronal plane and penetrated 1.5 mm into the surface of the telencephalon. The pipette, which was oriented vertically, was positioned based on trigonometric calculations so that the tip was located as close as possible to the 2 poles of the stimulating electrode. 2) Prelidocaine measures: A recording microelectrode was lowered into the pretectum, and the direction and spatiotemporal tuning of an LM neuron was characterized (see Visual stimulus presentation above), as was the response to electrical stimulation of the Wulst (see Orthodromic stimulation above). 3) Lidocaine was injected into the Wulst (2–4 µl) using a picospritzer (General Valve Corporation). Because the washout time of lidocaine is about 20 min (Sandkühler et al. 1987), supplemental injections of lidocaine were administered every 10 min to prolong the inactivation of the Wulst. 4) Postlidocaine measures: Five minutes after the initial injection of lidocaine, the response properties of the LM neuron and the effects of Wulst electrical stimulation were tested again. 5) Recovery measures: After the last application of the pharmacological blockade, lidocaine was allowed to wash out for 40–60 min, and the response properties of the LM neuron and the effects of electrical stimulation were tested a final time.
nBOR inactivation general procedure
The procedure to measure the effects of nBOR inactivation was as follows. 1) The nBOR was located based on stereotaxic coordinates (Karten and Hodos 1967), and the dorsal border of the nBOR was determined with extracellular recording. 2) The recording electrode was replaced with an injecting pipette filled with lidocaine (see Wulst inactivation general procedure above). The pipette was positioned such that the tip was at the approximate depth of the dorsal-most responsive nBOR cell from the recording track. 3) A bipolar stimulating electrode was positioned in the Wulst (see Wulst inactivation general procedure above). 4) A recording microelectrode was lowered into the pretectum, and the direction and spatiotemporal tuning of an LM neuron was characterized (see Visual stimulus presentation above), as was the response to electrical stimulation of the Wulst (see Orthodromic stimulation above). 5) Lidocaine (0.25–0.5 µl) was injected into the nBOR (for details see Wulst inactivation general procedure above). 6) Five minutes after the initial injection of lidocaine, the response properties of the LM neuron and the effects of Wulst electrical stimulation were tested again. 7) After the last application of the pharmacological blockade, lidocaine was allowed to wash out for 40–60 min, and the response properties of the LM neuron and the effects of electrical stimulation were tested a final time.
Technical considerations
The hyperstriatum accessorium (HA) and hyperstriatum intercalatus superior (HIS) of the pigeon Wulst extend 14.5–7.5 mm anterior of interaural zero, and are 
3–4 mm in the mediolateral and dorsoventral dimensions (Karten and Hodos 1967). The approximate volume of the HA and HIS combined is 40 mm3. Injection of the retrograde tracer Cholera Toxin Subunit B into the LM revealed that only a discrete population of neurons in the Wulst project to the pretectum (C. J. Ogilvie, N. A. Crowder, I. R. Winship, A. P. Nguyen, K. G. Todd, and D.R.W. Wylie, unpublished observations). The LM-projecting neurons form a dorsoventral strip located in the lateral margin of HA, along the boarder of HIS. In the rostrocaudal dimension, these cells extend from about 13.75 to 11.25 mm anterior to interaural zero. The approximate volume of the region containing the LM-projecting neurons is 10 mm3.
The effective spread of 1 µl of lidocaine was investigated by Sandkühler et al. (1987) and Martin (1991), and was estimated to have a radius of 1.4–1.7 mm (which translates to a volume of 11.5–20.6 mm3). Given that the effective spread of 1 µl of lidocaine is just enough to encompass the area of Wulst that projects to the LM, we are confident that 2–4 µl of lidocaine inactivated all afferents from the Wulst to LM.
Follett and Mann (1986) investigated the current spread of both monopolar and concentric bipolar electrodes. Extrapolating from the strength-spread and strength-duration curves provided by Follett and Mann (1986), we estimate that the effective current spread of a 400-µA pulse lasting 500 µs is 
2 mm. Furthermore, stimulation intensities of 100–400 µA certainly provide enough current spread to include the area of Wulst that projects to the LM. Thus the extent of the lidocaine block and the electrical stimulation (which confirms the efficacy of the block) spread through a large portion of the Wulst, and certainly included the Wulst neurons that project to the LM.
Histology
In some cases, a dye spot was left at the final recording site by iontophoretically injecting the Pontamine sky blue and NaCl from the recording electrode (+3 µA, 3 s ON/3 s OFF, for 20 min). 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, nBOR, and Wulst were collected. Sections were mounted onto gelatin chrome aluminum-coated slides and lightly counterstained with neutral red. The tissue was then examined using light microscopy to confirm the locations of electrode tracks and dye spots in the LM, and the stimulating electrode and lidocaine injecting pipette tracks in the Wulst.
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RESULTS |
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). Normal properties of LM neurons
All 45 LM neurons that were quantitatively examined for directional tuning exhibited direction selectivity. A unit was assigned a direction preference by calculating the maximum of the best cosine fit to the tuning curve. Twenty, 4, 5, and 16 LM neurons preferred forward (i.e., temporal to nasal), downward, backward, and upward motion, respectively. Of the 9 LM neurons tested with the handheld stimulus, 2, 4, 2, and 1, preferred forward, downward, backward, and upward motion, respectively. The predominance of neurons preferring forward motion is consistent with previous studies of the pigeon LM (Crowder et al. 2003,Crowder et al. 2003; Winterson and Brauth 1985; Wylie and Crowder 2000; Wylie and Frost 1996).
The spatiotemporal response properties of the 45 neurons were also quantitatively examined. Using SigmaPlot, contour plots were constructed where TF was on the ordinate, SF was on the abscissa, and the mean firing rate relative to the spontaneous firing rate (SR) was plotted on the z-axis. Given that motion in the preferred and antipreferred directions generally results in excitation and inhibition of the neuronal firing, respectively, we refer to excitatory response (ER) and inhibitory response (IR) plots (e.g., Figs. 5 and 7). The location of the peak in the contour plots was assigned quantitatively by fitting the primary peak in each contour plot to a 2-dimensional Gaussian function (Crowder et al. 2003,Crowder et al. 2003; Perrone and Thiele 2001). Consistent with previous studies of the pretectum (Crowder et al. 2003,Crowder et al. 2003; Ibbotson et al. 1994; Wylie and Crowder 2000), the peaks cluster into 2 quadrants: cells responding best to gratings of low SF/high TF (29 cells), or high SF/low TF (16 cells). Following Ibbotson et al. (1994), we refer to these as "fast" and "slow" cells, respectively.
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All 59 LM neurons that were tested with orthodromic stimulation of the Wulst showed a modulation in firing. The average stimulation threshold to elicit modulation was 65 µA (SD = 38 µA). Two distinct effects were observed after Wulst stimulation. One group of cells showed a short-latency excitation followed by longer-latency inhibition. The second group of cells showed only the longer-latency inhibition. We refer to these groups as W+ cells and W– cells, respectively. Figure 1 shows data from a W+ cell, including the average spike waveform (Fig. 1A), the effects of subthreshold (Fig. 1B; 25 µA), and suprathreshold stimulation (Fig. 1, C and D; 200 µA). Suprathreshold stimulation of the Wulst elicited a burst of 3–5 spikes at an average first-spike latency of 20 ms (SD = 1.6 ms). As expected with orthodromic stimulation, the average first-spike latency decreased as the current intensity increased (in this case from 21 ± 2.3 ms at 50 µA to 20 ± 1.6 ms at 200 µA). As shown in Fig. 1D, the excitatory burst was followed by a period of inhibition (at about 40–90 ms). At higher intensities, the effects of the stimulation were often manifested as oscillations between excitation and inhibition lasting up to 1 s (Fig. 1D). The consistency of the stimulation effect is shown in the raster plot and PSTH (Fig. 1D).
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Directional tuning, as determined by best fit to cosines, for 27 W+ and 18 W– neurons is shown in Fig. 3, A and B, respectively. The orientation of each line represents the direction preference of individual W+ (Fig. 3A) and W– (Fig. 3B) neurons. From this figure it is clear that there were no differences between W+ and W– cells with respect to their direction preferences. Figure 3C plots the locations of the primary ER peaks from the spatiotemporal contour plots of 27 W+ (empty circles) and 17 W– neurons (filled circles). Of the W+ cells, 18 were fast cells, and 9 were slow cells. Of the W– neurons, 11 were fast cells and 6 were slow cells. From Fig. 3C it is clear that there were no differences between W+ and W– cells with respect to their spatiotemporal tuning.
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The directional tuning and spatiotemporal response properties of 20 LM neurons were tested before, during, and after the Wulst was inactivated with lidocaine. The Wulst was inactivated for 1 h using multiple lidocaine injections (see METHODS). Of these 20 neurons, 13 were also tested with orthodromic stimulation from the Wulst before, during, and after the Wulst was inactivated with lidocaine. In all cases, Wulst inactivation completely eliminated all electrical stimulation effects. Moreover, full recovery of the stimulation effects was seen for every cell after the lidocaine was allowed to wash out. Figure 4 shows a W+ neuron before the Wulst was injected with lidocaine (Fig. 4A), a few minutes after the lidocaine injection (Fig. 4B), and after the lidocaine effect had washed out (Fig. 4C). This explicit reversible inactivation effect was evident for all 13 LM neurons that were tested with Wulst electrical stimulation.
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EFFECTS OF WULST INACTIVATION ON THE DIRECTION TUNING OF LM NEURONS. None of the LM neurons showed a significant change in direction preference after Wulst inactivation. Two neurons showed changes of 14 and 16°, whereas the direction change for other neurons did not exceed 6° (mean = 2.5°). The magnitude of modulation, both excitation and inhibition, remained unchanged for all neurons. Figure 5A shows the direction tuning of an LM neuron before (solid) and after (dashed) Wulst inactivation.
SPATIOTEMPORAL CHANGES AFTER WULST INACTIVATION. The spatiotemporal properties of all 20 LM neurons were examined before and during Wulst inactivation, and for 16 neurons after lidocaine washout. Inactivation of the Wulst did not significantly affect the spatiotemporal profiles of any LM neurons tested. Figure 5B shows the ER and IR plots of a single LM neuron before (Fig. 5B, left) and during (Fig. 5B, right) Wulst inactivation. In these plots excitatory peaks are shown in white and inhibitory peaks are shown in black. For the cell shown in Fig. 5B, both the ER plot prelidocaine (Fig. 5B, top left) and ER plot postlidocaine (Fig. 5B, top right) had a main peak at 1 cpd/0.5 Hz (+50 spikes/s), and a smaller peak at 0.06 cpd/16 Hz (30 spikes/s). Similarly, the IR plot prelidocaine (Fig. 5B, bottom left) and postlidocaine (Fig. 5B, bottom right) looked very similar, with a single inhibitory peak at 1 cpd/0.5 Hz (–16 spikes/s).
Effects of nBOR inactivation on the response properties of LM neurons
There is a reciprocal connection between the LM and nBOR (Azevedo et al. 1983; Brecha et al. 1980; Wylie et al. 1997). Because the Wulst also projects to the nBOR (Rio et al. 1983), we hypothesized that the longer-latency modulation of LM cells that resulted from Wulst stimulation might arise from the nBOR cells that are also activated by Wulst stimulation. To test this possibility, the effect of Wulst electrical stimulation on 4 LM neurons was measured before, during, and after the nBOR was inactivated with lidocaine. The direction and spatiotemporal response properties of these LM neurons were also measured during nBOR inactivation, serving to replicate the data presented by Crowder et al. (2003,2003), and confirm inactivation of the nBOR.
Figure 6 shows PSTHs from a W– neuron before the nBOR was injected with lidocaine (Fig. 6A), a few minutes after the lidocaine injection (Fig. 6B), and after the lidocaine washed out (Fig. 6C). Before nBOR inactivation, and after the lidocaine washout period, the W– neuron showed long-latency inhibition starting at 20 ms. When the nBOR was inactivated, this inhibition was strongly diminished. This decrease in long-latency inhibition was evident in 2 W+ cells and one W– cell. The remaining neuron was a W– cell that showed a lengthening in the duration of its long-latency inhibition (20–130 ms prelidocaine; 20–180 ms during lidocaine). The short-latency excitation shown by W+ cells was not affected by nBOR inactivation (not shown).
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DISCUSSION |
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; Miceli et al. 1979). We electrically stimulated the Wulst and found that LM neurons were either excited (W+ cells) or inhibited (W– cells). However, when the Wulst was temporarily inactivated by lidocaine neither the directional nor spatiotemporal response properties of LM neurons were affected. W+ and W– cells in the LM
This study is the first to demonstrate the effects of Wulst stimulation on the activity of pretectal neurons. Just over half of the LM neurons tested showed short-latency (13.5 ms) excitation to Wulst stimulation, whereas the remainder showed longer-latency (28.3 ms) inhibition to Wulst stimulation. We refer to these LM neurons as W+ cells and W– cells, respectively. Wulst stimulation effects did not appear to correlate with directional or spatiotemporal tuning. The bimodal distribution of latencies for W+ and W– neurons suggests a direct and indirect route from the Wulst to the LM. The short-latency excitatory stimulation effects seen in LM W+ neurons likely arise from the monosynaptic inputs they receive from the Wulst (Gottlieb and McKenna 1986; Miceli et al. 1979; Rio et al. 1983). Longer-latency inhibitory effects could be the result of polysynaptic feed-forward or even feed-back circuits within the LM itself or the result of feed-forward inhibitory projections from other pretectal nuclei also receiving Wulst input (see following text).
W+ and W– cells in the nBOR
Nogueira and Britto (1991) examined the effects of Wulst stimulation on the firing rate of nBOR neurons. Their findings were strikingly similar to those of the present study: nBOR neurons showed either a short-latency excitation (26%; average latency = 13 ms) or a longer-latency inhibition (38%; average latency = 35 ms). Clearly the nBOR has counterparts to the W+ (average latency = 13.5 ms) and W– (average latency = 28.3 ms) LM cells described in the present study. This argues for a similar function of the telencephalic projection to the pretectum and AOS.
Longer-latency modulation of LM neurons from Wulst stimulation: Wulst, LM, nBOR interactions
The initial longer-latency inhibition of the W– cells in response to Wulst stimulation, as well as the longer-lasting inhibitory/excitatory oscillations seen in both W+ and W– neurons, could arise from inhibitory interneurons in the pretectum and/or from Wulst stimulation following an indirect route through the nBOR (Brecha et al. 1980; Clarke 1977; Gamlin and Cohen 1988b; Wylie et al. 1997). When we inactivated nBOR, the long-latency modulation in response to Wulst stimulation was clearly affected. For 3 of 4 cases, there was a reduction in long-latency inhibition, and in one case there was an increase. It has been suggested that the projection from the nBOR to LM is predominantly inhibitory (Baldo and Britto 1990; van der Togt and Schmidt 1994), but also excitatory (Baldo and Britto 1990; Crowder et al. 2003,Crowder et al. 2003). Oscillations seen in some LM neurons after electrical stimulation are likely attributable to the delicate balance in reciprocating activity between the nBOR and LM. Nogueira and Britto (1991), who examined the effects of Wulst stimulation on the activity of nBOR neurons (see above), came to an identical conclusion. They suggest that short-latency stimulation effects arise from direct Wulst input to the nBOR, whereas the longer-latency effects result from stimulation of the LM, which projects to the nBOR.
Function of the Wulst projection to the LM
Neurons in the LM show clear directional tuning (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) and are also tuned in the spatiotemporal domain (Ibbotson and Price 2001; Wylie and Crowder 2000). Furthermore, it has been shown that input from the nBOR affects the spatiotemporal tuning (but not direction preference) of LM neurons (Crowder et al. 2003,Crowder et al. 2003). In addition to the nBOR, the Wulst represents another prominent source of extraretinal input to the LM. In this study, the Wulst was temporally inactivated with lidocaine to determine the function of the projection from Wulst to LM. Although Wulst inactivation altered the spontaneous rate of some LM neurons, it had no effect on the directional or spatiotemporal tuning of LM neurons. Despite the fact that we have negative findings in this regard, we have a very clear positive control: in every case where electrical stimulation was used (and as shown in Fig. 4), lidocaine injection did inactivate the input from the Wulst to the LM.
In a pair of studies investigating the function of the projection from the Wulst to the nBOR, Britto and colleagues (Britto et al. 1990; Hamassaki et al. 1988) argued that the Wulst contributes to the directional tuning of nBOR neurons. They compared the distribution of preferred directions in normal pigeons versus those that had the Wulst removed by aspiration. They observed that the proportion of neurons preferring upward motion was reduced and the proportion of neurons preferring temporal-to-nasal motion was increased in the group with Wulst lesions. Given the results of the present study, these previous findings are difficult to reconcile. One could conclude that the Wulst contributes to directional tuning of nBOR neurons, but not LM neurons. However, this explanation is unsatisfactory because the electrical stimulation of the Wulst results in similar modulation of nBOR and LM units (Nogueira and Britto 1991; present study). We suggest that there is an inherent problem with the between-groups design used by Hamassaki et al. (1988) and Britto et al. (1990) insofar as the differences observed could represent a sampling bias. In fact, their control groups suggest that perhaps this is the case. From Fig. 2 of Britto et al. (1990), most of the nBOR neurons in the control group preferred upward or downward motion, but neurons preferring nasal-to-temporal motion were absent. However, 3 different labs have found that nBOR in normal pigeons contains equal proportions of neurons preferring upward, downward, and nasal-to-temporal motion (Gioanni et al. 1984; Wylie and Frost 1990; Zhang et al. 1999; see also Rosenberg and Ariel 1990). This possible sampling bias is not an issue in within-subject designs such as reversible inactivation studies. It is likely that this issue will not be resolved until the reversible inactivation methods used in the present study are applied to the nBOR. Under these circumstances, visual response properties of single nBOR units could be tested before and after the inactivation of the Wulst. Indeed, Nogueira and Britto (1991) themselves stated that reversible inactivation studies are needed to precisely evaluate the effect of visual Wulst on nBOR neurons.
If the Wulst does not contribute to the directional or spatiotemporal tuning of LM neurons, what is the function of this projection? The Wulst is considered to be a homolog of mammalian primary visual cortex based on embryological, histochemical, and physiological characteristics (Karten and Shimizu 1989; Karten et al. 1973; Medina and Reiner 2000). This excludes the rostral tip of the Wulst, which is somatosensory (Medina and Reiner 2000; Wild 1987). Like V1, neurons in the visual Wulst have small receptive fields and are thought to be involved in form vision. Many respond to small moving stimuli, and there is evidence of orientation tuning, binocularity, and columnar organization (Liu and Pettigrew 2003; Miceli et al. 1979; Pettigrew and Konishi 1976; Revzin 1969; Wilson 1980). In owls, the visual Wulst appears to play a major role in the processing of binocular vision and higher-level visual stimuli such as subjective contours (Neider and Wagner 1999; Pettigrew 1979; Porciatti et al. 1990). However, even large lesions to the Wulst produce surprisingly few visual deficits in pigeons (e.g., Hodos et al. 1984; Pritz et al. 1970; Riley et al. 1980). If the LM-projecting neurons in the Wulst are involved in form vision, it is possible that the projection from the Wulst to the pretectum and AOS is to adjust the gain of a subset of optic flow sensitive neurons when the animal is attending to small objectlike stimuli.
It is also possible that the Wulst neurons that project to the LM are somatosensory or somatosensory/visual neurons. First, Deng and Wang (1992, 1993) demonstrated that there is significant overlap between areas of the Wulst that process visual and somatosensory information, with some neurons even responding to both visual and somatosensory stimuli (also see Medina and Reiner 2000). Second, from our own observations, the area of the Wulst containing the LM-projecting neurons does overlap with the area in which somatosensory responses are evoked (Deng and Wang 1992, 1993; Wild 1987). Somatosensory information such as air passing through the pigeon's feathers could be used in addition to optic flow information to analyze self-motion. In support of this idea, neurons classified as bimodal (visual and somatosensory) as well as trimodal (visual, somatosensory, and vestibular) have been found in the ventral intraparietal area (VIP) of macaque monkeys, which along with the middle superior temporal area (MST) is responsible for the cortical processing of optic flow in primates (Bremmer et al. 2000). These ideas suggest that perhaps LM neurons are modulated by somatosensory stimulation and that inactivation of the Wulst would block this modulation.
Function of the telencephalic input to the pretecum and AOS in mammals
The presence of a telencephalic projection on the AOS and pretectum appears to be highly variable among both lateraleyed and frontal-eyed species. For example, the pretectum receives cortical afferents in frontal-eyed species such as cats and monkeys (Hoffmann et al. 1991; Ilg and Hoffmann 1993; Mustari et al. 1994; Schoppmann 1981), but not opossums (Pereira et al. 2000). In lateral-eyed animals, the NOT receives cortical input in rats (Shintani et al. 1999), guinea pigs (Lui et al. 1994), and rabbits (Hollander et al. 1979), but not in hamsters (Lent 1982) or tree shrews (Huerta et al. 1985). Electrophysiological, behavioral, and developmental studies in cats have suggested that the cortical projection to the AOS and pretectum alters the gain asymmetries of vertical and horizontal optokinetic nystagmus as an adaptation to frontal eye placement (Grasse and Cynader 1986, 1987, 1988, 1990). Because the pigeon is a lateral-eyed animal, and the telencephalic inputs to the LM do not affect the directional tuning of these neurons, this projection likely serves a different purpose than in the cat.
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ACKNOWLEDGMENTS |
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This research was supported by grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada to D.R.W. Wylie and C. T. Dickson. D.R.W. Wylie was supported by the Canada Research Chairs Program (Tier II). C. T. Dickson was supported by the Alberta Heritage Foundation for Medical Research (AHFMR) Scholars Program and N. A. Crowder was supported by a Julie Payette NSERC postgraduate scholarship.
Present address of N. A. Crowder: Australian National University Visual Sciences Group, Research School of Biological Sciences, Canberra ACT 2601, Australia.
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FOOTNOTES |
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Address for reprint requests and other correspondence: D. R. Wong-Wylie, Department of Psychology, University of Alberta, Edmonton, Alberta T6G 2E9, Canada (E-mail: dwylie{at}ualberta.ca).
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