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Exp Brain Res (2000) 133:209–218 Digital Object Identifier (DOI) 10.1007/s002210000374 R E S E A R C H A RT I C L E Sabine Sudkamp · Matthias Schmidt Response characteristics of neurons in the pulvinar of awake cats to saccades and to visual stimulation Received: 6 September 1999 / Accepted: 10 February 2000 / Published online: 31 March 2000 © Springer-Verlag 2000 Abstract We studied responses of pulvinar neurons in awake cats that were allowed to execute spontaneous eye movements. Extracellular cell activity during saccades, saccade-like image shifts, and various stationary visual stimuli was recorded together with the animals’ eye positions. All neurons analyzed had receptive fields that covered most of the central 80×80° of the animals’ visual field and did only respond to large (>20°) visual stimuli. According to their response properties, recorded neurons were divided into three populations. The first group, termed “S neurons” (16%), responded when the animals performed saccades but were unresponsive to any of the visual stimuli tested. These neurons do not seem to receive a visual input that is strong enough to drive them. The second group, termed “V neurons” (51%), responded to various visual stimuli including saccade-like image motion when the eyes were stationary, but not when the animals executed saccades. V neurons therefore distinguish retinal image movements that are generated externally from internally generated image motion. Finally, “SV neurons” (31%) responded when the animals made saccades as well as to saccade-like image motion or to stationary stimuli. Although these neurons do not distinguish self-induced retinal image motion from motion generated by external stimulus movements, they must receive non-retinal motion-related input, because responses elicited by saccades had shorter latencies than responses to saccade-like stimulus movements. Only SV neurons resemble response properties of pretectal neurons that project to the pulvinar and that comprise the major subcortical visual input. The functional significance of pulvinar neuronal populations for visual and visuomotor information processing is discussed. S. Sudkamp · M. Schmidt (✉) Allgemeine Zoologie and Neurobiologie, Ruhr-Universität Bochum, 44780 Bochum, Germany e-mail: [email protected] Tel.: +49-234-3227709, Fax: +49-234-3214278 Key words Extrageniculate visual thalamus · Pretectal nuclear complex · Saccadic eye movements · Visuomotor integration Introduction In higher mammals visual information from the retina can reach the visual cortex either directly, via the dorsal lateral geniculate nucleus (LGNd), or by a more indirect pathway, via the superior colliculus and pretectal nuclear complex to the lateral posterior-pulvinar complex (LP-P) which in turn is reciprocally connected with many visual cortical areas. While the functional role of the geniculostriate pathway has been elucidated by many investigators, knowledge about the function of the extrageniculostriate pathway is far from complete. In cats, the LP-P consists of three different subnuclei. Each of them is characterized by specific afferents from visual structures that are almost restricted to it. Tectal afferents terminate mainly in the medial division of the lateral posterior thalamic nucleus (LPm), the lateral division of LP (LPl) is reciprocally connected with area 17 and 18, and a pretectal projection mainly ends in the pulvinar (Pul; Graybiel and Berson 1980; Abramson and Chalupa 1988). In addition to these specific afferents, all three subnuclei share multiple cortical areas as common input sources, in particular various extrastriate visual areas (Updyke 1977, 1981; Berson and Graybiel 1978; Graybiel and Berson 1980; Abramson and Chalupa 1985). Physiological studies of visual responses of LP-P neurons in cat, monkey, and rabbit have almost exclusively focused on the integration of tectal and cortical information. Thus, a number of studies have addressed response properties of neurons in cat and rabbit LPm and LPl, and in tecto-recipient portions of the Pul in monkey (cat: Fish and Chalupa 1979; Berson and Graybiel 1983; Abramson and Chalupa 1985, 1988; Chalupa and Abramson 1988, 1989; Chalupa 1991; Casanova et al. 1997; Merabet et al. 1998; behaving monkey: Robinson and McClurkin 1989; Robinson et al. 1991; rabbit: 210 Casanova and Molotchnikoff 1990). In contrast, physiological data from neurons in the pretecto-recipient Pul is rather limited (cat: Godfraind et al. 1972; Mason 1981). Receptive fields in the LPl and LPm mostly have welldefined borders and LP neurons often respond, directionally or orientationally selective, to motion of small visual stimuli. In contrast, receptive fields in the Pul are often very large, do not have clear borders, and Pul neurons respond to diffuse illumination changes rather than to small visual stimuli (Godfraind et al. 1972; Mason 1981; Chalupa and Abramson 1988, 1989; Casanova et al. 1989). As noted above, the primary subcortical visual input to the Pul originates from the pretectal nuclear complex. Following the nomenclature introduced by Guillery et al. (1980), we regard the narrow band of retinal terminations shown by several authors (see, for example, Itoh et al. 1979; Leventhal et al. 1980) at the caudoventral border of the Pul as part of the medial interlaminar nucleus and not as part of the Pul. Pretectal neurons that project to the Pul are distributed throughout the whole superficial pretectum (Weber et al. 1986; Kubota et al. 1988). Studies in anesthetized cats have demonstrated that these neurons have large receptive fields (diameter >40°) and that the majority of them respond with short bursts to rapid displacements of a large random square pattern and to brief light flashes (Sudkamp and Schmidt 1995). They are thought to be identical with so-called “jerk” neurons that respond, as known from awake cats, with short bursts not only to rapid image shifts while the eyes are stationary but also when saccadic eye movements are executed in the light (Schweigart and Hoffmann 1992). It is not known yet how this pretectal input is further processed in the Pul because response properties of Pul neurons in awake cats so far have not been described. However, Pul neurons that respond after saccadic eye movements have been described in encéphale isolé cats (Infante and Leiva 1984). In primates, one function discussed for Pul neurons is the spatial control of visual attention (Ungerleider and Christensen 1979; Desimone et al. 1990) possibly by enhancing responses to new visual stimuli that appear in a complex environment (Petersen et al. 1985; Robinson et al. 1986; Desimone et al. 1990; Desimone and Duncan 1995). The signal necessary for this enhancement could be generated by a saccade-related activation of Pul neurons that are involved in the processing of oculomotor information rather than in object analysis tasks. The analysis of saccade-related responses of single neurons therefore is a first step in order to elucidate the possible role of the cat Pul in visual and visuomotor processing. Here we report on response properties of single units to visual stimuli and during saccadic eye movements in awake cats. Materials and methods Animals Experiments were conducted on six young adult male and female cats with body weights between 2.7 and 4.7 kg. All experimental procedures were done in strict compliance with governmental regulations and in accordance with the Guidelines for the Use of Animals in Neuroscience Research of the Society for Neuroscience. Animal preparation For initial surgery, cats were anesthetized with ketamine (20 mg/kg body weight) and thiazine hydrochloride (1 mg/kg body weight). Under additional local anesthesia by lidocaine hydrochloride, the trachea was intubated to allow artificial respiration with a mixture of 66% nitrous oxide, 32% oxygen, and 2% carbon dioxide, supplemented by 0.4–1% halothane. Additional doses of ketamine were administered if necessary. Respiration volume was regulated to an end tidal volume of 4% carbon dioxide. The body temperature was automatically maintained at 37.5°C. Carbon dioxide level in expired air, endotracheal pressure, and body temperature were continuously monitored during surgery. Throughout anesthesia, animals were given an intravenous infusion of 5% glucose in 0.9% NaCl. A craniotomy was performed above the Pul at HorseleyClarke stereotaxic coordinates taken from Reinoso-Suarez (1961). A recording cylinder centered at A6.5/L6 and three anchor screws were fixed to the scull with dental acrylic cement. In order to measure eye movements, a scleral search coil was implanted in one eye according to the method of Judge et al. (1980). During the 1st week after surgery, animals were given 60 mg chloramphenicol per day to prevent infections. Recording Daily recording sessions started 7 days after surgery and typically lasted for 1–2 h. Cats were placed in a wooden box to limit body movements and their head was restrained by a head holder fixed to the box. Horizontal and vertical eye movements were monitored using the phase-detection principle in a magnetic field (Kasper and Hess 1991). Eye movements were measured relative to the stationary head. Extracellular single unit activity in the LP-P was recorded with tungsten-in-glass electrodes fixed to a holder that was mounted on top of the recording cylinder. A micromanipulator attached to the electrode holder allowed electrode penetrations in a 10×10-mm area around the center of the recording cylinder. The electrodes were advanced through the intact dura by a hydraulic microdrive. Signals were conventionally amplified, band-pass filtered, and digitally stored for off-line analysis. Extracellular responses were collected either while the cat executed spontaneous saccades in front of a stationary random square pattern and in total darkness, or during visual stimulation when the eye was stationary. Visual stimuli were projected onto a tangent screen 30 cm in front of the cat that covered the central 80×80° of the visual field. The most common visual stimulus was a random square pattern (pixel size 2.5°, luminance of light squares 20 cd/m2, luminance of dark squares 3 cd/m2) that was either moved in a saccade-like fashion to elicit saccade-like retinal image shifts or that was flashed on and off at 0.5 Hz. Because the size of the stimulus exceeded that of the tangent screen, no moving edges occurred when the stimulus was moved. Small stimuli, such as single light or dark spots or bars were also tested, however, such stimuli were not effective in eliciting neuronal responses (see Results). At the end of the final recording session of each individual animal, the recording sites were marked by electrolytic microlesions in three penetrations where neurons had been successfully recorded in prior session. Recording sites of all recorded neurons were reconstructed from the lesions in 50-µm-thick coronal sections stained with cresyl violet (Fig. 1). 211 Fig. 1 Photomicrograph of a cresyl violet-stained frontal section through the left cat thalamus. Two electrolytic microlesions (black arrows) mark one of the electrode penetrations in the pulvinar (Pul); another electrode track is seen more lateral (white arrows). LGNd Dorsal lateral geniculate nucleus, LPl lateral posterior nucleus, lateral part, LPm lateral posterior nucleus, medial part. Scale bar 2 mm Data analysis For saccade detection, eye velocity was calculated off-line from the eye position data. A saccade was detected when the eye velocity exceeded 50°/s and its amplitude exceeded 2°. Saccade onset and saccade end were defined as the time when velocity reached 10% or dropped below 10% of the peak velocity during the saccade. Average saccade velocity, duration, amplitude, and direction were calculated from the horizontal and vertical eye position values between saccade onset and saccade end. Neuronal responses were analyzed on the basis of peristimulus time histograms triggered to either saccade or stimulus onset. A neuronal response was regarded as significant if cell activity was significantly different (P<0.05) from average spontaneous activity in a time window of at least 200 ms prior to saccade or stimulus onset. If responses to at least 25 stimulus sweeps or saccades had been collected, a t-test was used to determine significance; for less than 25 sweeps a Mann-Whitney rank sum test was used. Responses were characterized by the latency to half of the peak activity, response duration, and average activity. Results In the LP-P of six awake cats, 169 units could be characterized by their responses to visual stimuli or to saccades. Reconstruction of electrolytic lesions showed that the great majority of them were located in the Pul (n=125). The remaining 44 neurons were located in adjacent nuclei [LPl, LPm, and lateral intermediate nucleus, caudal part]. Because the animals executed voluntary eye movements, saccades to which responses were analyzed covered all possible directions and varied considerably in size (2.0–48.7°, mean 8.0±6.0°, n=1499). To allow comparison of saccade-evoked with stimulus-evoked neuronal responses, we used a standard 8° horizontal stimulus shift with a duration of 100 ms, referred to as ‘saccadelike stimulus’, to achieve an image shift on the retina that was similar to an average saccade. Recorded neurons could generally be divided into three response groups: first, neurons that responded dur- ing saccades but not to visual stimulation (n=27, 16% of characterized neurons; S neurons), second, neurons that responded to visual stimuli but not during saccades (n=86, 51% of characterized neurons; V neurons), and third, neurons that responded during saccades and to visual stimuli (n=53, 31% of characterized neurons; SV neurons). Three neurons (2%) remained unclassified because no saccades occurred when they were recorded. Neurons of either group were distributed throughout the whole Pul. While no significant difference was found in the distribution of V and SV neurons, S neurons tended to be more frequent in the rostral half of the Pul. Neurons recorded outside the Pul could belong to either response group (Fig. 2). S neurons The response of a typical S neuron is shown in Fig. 3. This neuron was activated whenever the animal executed a saccade in light and in total darkness but it did not respond to any of the visual stimuli used. The response characteristics to saccades in the light of 22 S neurons located inside the Pul are summarized in Table 1. Five of the 8 neurons that were also tested for saccade responses in total darkness showed saccadic responses that were not significantly different from responses in light (Table 1). Responses of S neurons found outside the Pul were not significantly different from those located inside the Pul (Mann-Whitney rank sum test, P>0.05). Thus, S neurons both inside and outside the Pul most likely receive saccade-related input of either motor, premotor, or proprioceptive origin. If they do also receive visual input, that input is not strong enough to drive them. In all cases tested, the S neurons’ saccade response latency, duration, or amplitude did neither correlate to saccade direction (n=4), nor to saccade amplitude, duration, or eye velocity (n=12). 212 Fig. 2 Distributions of S neurons (A), V neurons (B), and SV neurons (C) in cat thalamus. Two series of reconstructed frontal sections, arranged from caudal to rostral (bottom left to top right) are shown for each population. For better identification, the Pul is indicated by the gray shading. Each black dot represents a single recorded neuron. LGNd Dorsal lateral geniculate nucleus, LD lateral dorsal nucleus, LIc lateral intermediate nucleus, caudal part, LPl lateral posterior nucleus, lateral part, LPm lateral posterior nucleus, medial part, MGB medial geniculate body, SN substantia nigra Fig. 3 Responses of a representative S neuron to saccades in light (A), saccades in darkness (B), saccade-like stimulus shifts (C), light on (D), and light off (E) shown as peristimulus time histograms. Eye position traces above histograms in A and B were calculated from recorded horizontal and vertical eye positions, stimulus position is indicated above histogram in C, and stimulus luminance is indicated above histograms in D and E. Saccade or stimulus onset is always at time ‘0’. The calibration bar at eye position traces in A and B represents 20°, binwidth of PSTHs, 5 ms V neurons The response of a typical V neuron is shown in Fig. 4. This neuron was not activated by saccades but it responded to saccade-like image shifts with a response latency of 40 ms, and to On-Off stimuli with a latency of 35 ms. Responses to saccade-like image shifts of large visual stimuli or to whole-field On-Off stimuli were a common feature of all V neurons; small stimuli such as dots or bars had no effect. However, only 19 of 64 V neurons (30%) tested responded to both saccade-like image shifts and On-Off stimuli, 32 V neurons (50%) responded only to On-Off, and 13 V neurons (20%) responded only to saccade-like image shifts. Twenty-three V neurons that responded to saccade-like image shifts were not tested with On-Off stimuli. We did not further differentiate between these subgroups of V neurons be- 213 Table 1 Response properties of pulvinar (Pul) neurons to saccades and to visual stimuli. (n.r. No response, by definition) Responses to: S neurons V neurons SV neurons Inside Pul Outside Pul Range Median Range Median Range Median Range Saccades in light Latency (ms) Duration (ms) Amplitude (spk/s) 0–140 35–240 25–142 63 105 56 n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. 0–110 15–320 15–313 55 95 74 Saccades in darkness Latency (ms) Duration (ms) Amplitude (spk/s) 50–195 25–170 38–151 75 105 66 n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. 50–145 60–400 44–200 100 95 84 Saccade-like stimulus Latency (ms) Duration (ms) Amplitude (spk/s) n.r. n.r. n.r. n.r. n.r. n.r. 30–190 15–270 30–246 75 55 60 35–80 10–100 18–226 50 45 99 30–200 15–185 24–280 45 60 81 On stimulus Latency (ms) Duration (ms) Amplitude (spk/s) n.r. n.r. n.r. n.r. n.r. n.r. 20–115 10–150 19–314 48 35 86 20–75 10–100 28–320 40 25 182 25–90 20–100 22–222 43 50 114 Off stimulus Latency (ms) Duration (ms) Amplitude (spk/s) n.r. n.r. n.r. n.r. n.r. n.r. 25–120 15–200 11–198 58 35 54 20–100 10–70 22–245 30 30 162 25–80 10–170 51–215 40 43 105 cause no differences in their response characteristics were encountered (Table 1). However, a significant difference between V neurons inside and outside the Pul was noticed. Response latencies of V neurons outside the Pul to saccade-like stimulus shifts (35–80 ms, median 50 ms), to On (20–75 ms, median 40 ms), and to Off stimuli (20–100 ms, median 30 ms) were significantly shorter than for neurons inside the Pul (Mann-Whitney rank sum test, P<0.05). Also, response activities to saccade-like stimulus shifts (18–226 spk/s, median 99 spk/s), to On (28–320 spk/s, median 182 spk/s), and to Off stimuli (22–245 spk/s, median 162 spk/s) of V neurons outside the Pul were significantly higher than activities of neurons inside the Pul (Mann-Whitney rank sum test, P<0.05). SV neurons The response of a typical SV neuron is shown in Fig. 5. The neuron responded to saccades in light with a latency of 30 ms, but it did not respond to saccades in total darkness. Saccade-like image shifts elicited a response with a latency of 40 ms and On-Off stimulus responses had latencies of 35 ms and 40 ms, respectively. Responses to saccades and large visual stimuli, such as saccade-like image shifts or whole-field On-Off stimuli, were a common feature of all SV neurons. Small stimuli such as dots or bars were not effective in driving SV cells. Most SV neurons (n=53, 51%) responded to saccades and to saccade-like image shifts as well as to OnOff stimuli, 5 SV neurons (10%) responded only to sac- Median cades and saccade-like image shifts, and 12 SV neurons (23%) responded only to saccades and On-Off stimuli. The remaining 9 neurons (16%) responded during saccades and saccade-like image shifts but were not tested to On-Off. We did not further differentiate between these subgroups, because no differences in their response characteristics were encountered. There was also no significant difference between SV neurons inside the Pul and outside the Pul (Mann-Whitney rank sum test, P>0.05). Response parameters of SV neurons to saccades are summarized in Table 1. In 28 neurons tested, no significant correlations were found between response parameters and saccade amplitude, duration, and velocity. Furthermore, similar to what we found for S neurons, saccade responses of SV neurons (n=14) were independent from saccade direction. Five out of 26 SV neurons tested exhibited significant responses to saccades in darkness. While response latencies to saccades in darkness were significantly longer than those to saccades in light, both response amplitudes and response durations were similar to those observed in light (Table 1). Thirty-nine SV neurons (30 inside Pul, 9 outside) responded to saccade-like stimulus displacements. Thirty-five SV neurons responded to On (30 in Pul, 5 outside) and 32 SV neurons responded to Off stimuli (27 in Pul, 5 outside). Saccade responses vs visual responses From the response properties of SV neurons the question arises, whether the saccade-related responses observed 214 Fig. 4 Responses of a representative V neuron to saccades in light (A), saccade-like stimulus shifts (B), light on (C), and light off (D) shown as peristimulus time histograms. Eye position traces above histograms in A were calculated from recorded horizontal and vertical eye positions, stimulus position is indicated above histogram in B, and stimulus luminance is indicated above histograms in C and D. Saccade or stimulus onset is always at time ‘0’. The calibration bar at eye position traces in A represents 30°, binwidth of PSTHs, 5 ms are entirely elicited by the retinal image shift that occurs during saccades, or whether an additional non-visual component is present. A comparison of the parameters of responses to saccades with responses to saccade-like image displacements (Table 1) revealed no significant difference (Mann-Whitney rank sum test). Because the animals executed spontaneous saccades of variable amplitudes and durations, responses to saccades and responses to saccade-like image displacements were normalized to constant duration and accumulated (Fig. 6) to allow a better comparison. In the histograms shown in Fig. 6, Fig. 5 Responses of a representative SV neuron to saccades in light (A), saccades in darkness (B), saccade-like stimulus shifts (C), light on (D), and light off (E) shown as peristimulus time histograms. Eye position traces above histograms in A and B were calculated from recorded horizontal and vertical eye positions, stimulus position is indicated above histogram in C, and stimulus luminance is indicated above histograms in D and E. Saccade or stimulus onset is always at time ‘0’. The calibration bar at eye position traces in A and B represents 30°, binwidth of PSTHs, 5 ms saccade or stimulus onset is set at bin 20, saccade or stimulus end is set at bin 40. The bottom histogram shows the difference between the cumulative normalized histograms of responses to saccade and to image shifts. Because normalized saccade responses start at saccade onset while responses to image displacement begin at bin 215 significant (Mann-Whitney rank sum test, P<0.01). These differences indicate that saccade responses contain a non-visual component in addition to the visual component. Discussion Fig. 6 Population response of SV neurons to saccades (A) and to saccade-like stimulus shifts (B) normalized to equal durations. Saccade or stimulus onset is always at bin 20, saccade and stimulus end is always at bin 40 (both marked by stars), regardless of individual saccade duration. Eye position traces in A were calculated from recorded horizontal and vertical eye positions and normalized to equal durations, and stimulus position is indicated above histogram in B. The histogram in C shows the difference between A and B. The calibration bar at eye position traces in A represents 50° 30, an initial positive peak appears in the difference histogram. Later, the response to the visual stimulus is higher in amplitude, so the difference becomes negative. Furthermore, saccade responses end soon after saccade offset at bin 45, whereas responses to saccade-like image shifts continue until bin 53. The observed differences between bin 20 and 30 and between bin 45 and 53 were Neurons in the Pul of awake cats showed three different activation patterns in response to spontaneous saccades or to moving and stationary visual stimuli. A first group was only activated when the animal performed a saccadic eye movement, and this group of neurons was termed S neurons. A second group, V neurons, was activated by visual stimulation but did not respond to eye movements. A third group responded to both saccadic eye movements and visual stimulation and was termed SV neurons. A common feature of all Pul neurons that were responsive to visual stimulation, however, was the ineffectiveness of small stimuli (diameter <5°), such as light or dark spots or bars, to elicit any response. In earlier studies of the cat LP-P, both neurons with well-defined visual receptive fields that respond to relatively small stimuli and neurons with large receptive fields without clearly defined borders that respond to diffuse illumination have been described (Godfraind et al. 1972; Mason 1981; Chalupa and Abramson 1988, 1989; Casanova et al. 1989). However, neurons of the two groups are not distributed homogeneously throughout the LP-P. Instead, neurons with well-defined receptive field boundaries are predominantly found in the LP, while neurons with diffuse receptive fields are most prominent in the Pul (Godfraind et al. 1972; Mason 1981). Our results confirm these findings insofar as we recorded neurons with diffuse receptive fields that respond to very large stimuli inside the Pul. However, in contrast to both Godfraind et al. (1972) and Mason (1981), we did not find any neuron with clearly defined receptive field borders inside the Pul that responded to small bars or spots. It cannot be ruled out that this discrepancy is due to methodological differences. We tested visual responses in the Pul of awake cats that had not been trained to fixate. Under this condition it is impossible to test the entire visual field with small stimuli because cats make saccades to such stimuli and we therefore may have missed neurons that respond to small visual stimuli. Comparison of SV with S and V neurons Saccade responses were a common feature of S and SV neurons. For both cell classes no saccade parameters were encoded in saccade-related responses. Response latencies, response durations, or average response amplitudes were not significantly different between S and SV neurons. However, saccade responses of S neurons did not have a visually evoked component whereas in SV neurons the visual response component was always stronger than the non-visual component. Therefore, 216 S neurons and SV neurons most likely comprise neuronal populations that are independent from each other and that are also different functionally. V neurons and SV neurons may seem more similar because both neuronal populations responded to identical visual stimuli. However, in addition to the distinction in their responses to saccades, there are two further significant differences between V neurons inside the Pul and SV neurons. Firstly, response latencies of SV neurons to saccade-like image shifts were significantly shorter than those of V neurons. Secondly, average response amplitudes of SV neurons to On-Off stimuli are significantly larger than in V neurons (Mann-Whitney rank sum test, P<0.05). Therefore, it seems likely that SV and V neurons are also separate neuronal populations in cat Pul. Responses to saccades Saccade-related responses of cat LP-P neurons have been described in encéphale isolé cats that had their eyes covered by dark contact lenses (Infante and Leiva 1984). Under this condition, response latencies varied between 50 and 250 ms after saccade onset (mean 100 ms). We found similar response latencies for S and SV neurons to saccade onset in darkness. However, we observed shorter response durations and higher average response rates for both SV and S neurons (Table 1) than those described by Infante and Leiva (1984), i.e., 200–500 ms and 8–87 spk/s, respectively. Even more significant, in contrast to Infante and Leiva (1984) who reported saccade responses in LP-P to depend on saccade direction in their experimental condition, we did not detect any directional selectivity of saccade responses. It seems likely that these differences result from the different types of preparations. Comparison with monkey data We have grouped neurons in cat Pul into S, V, and SV responses according to their specific responses to saccades and to various visual stimuli. Similar response types have been described in monkey Pul nucleus: approximately half of the neurons that show excitatory responses during saccades also respond to visual stimuli and thus correspond to SV neurons. The remaining half of neurons does not show visual responses and can thus be classified as S neurons (Robinson et al. 1991). Some but not all S neurons as well as some but not all SV neurons in monkey Pul do also respond to saccades in total darkness, which is another similarity to our S and SV neurons. Finally, Robinson et al. (1991) found neurons that respond to bars that are moved when the eye is stationary, but that do not respond to the same retinal image movement when a saccade is made across a stationary bar. Such neurons may correspond to our V neurons in cat Pul. Comparison with pretectal neurons that project to the Pul Because the main visual input to the Pul in cat originates from the ipsilateral and, to lesser extent, contralateral pretectal nuclear complex, the question arises whether response properties of Pul neurons reflect this input. Pretectal neurons that project to the LP-P have large receptive fields and, in anesthetized cats, respond to On-Off stimuli and during saccade-like shifts of large patterns (Sudkamp and Schmidt 1995). These neurons show mean response latencies to saccade-like image shifts of 57 ms, mean response durations of 47 ms, and mean response rates of 169 spk/s. In behaving cats, pretectal cells have been described, that show similar response properties to visual stimuli and that display remarkable saccade-related responses (Schweigart and Hoffmann 1992). The similarities between the two neuronal groups recorded in anesthetized and awake cats have led to the conclusion that they are identical (Sudkamp and Schmidt 1995). Thus, as pretectal neurons that project to the Pul respond to both visual stimulation and to saccades, it seems reasonable to assume that the response properties of SV neurons in the Pul are generated by pretectal input. Since the mean conduction time of electrically evoked spikes from the pretectum to LP-P was 1.7 ms (Sudkamp and Schmidt 1995), the response latencies of SV neurons are compatible to a direct pretectal input, as are response durations and response amplitudes. If the pretectal input to the Pul provides the predominant visual input to SV cells, the underlying projection must be excitatory in nature. This is reasonable to assume, even though pretectal cells that project to the LGNd have been shown to be GABAergic (Cucchiaro et al. 1991; Wahle et al. 1994), because pretectal neurons that project to the Pul are independent from those that project to the LGNd (Sudkamp and Schmidt 1995). Interestingly, both projections, though anatomically independent, seem to share the functional property of transferring saccade-related information to their target structures (Schmidt 1996; Fischer et al. 1998). All the similarities in response properties between pretectal and SV Pul cells, of course, do not rule out the possibility that cortical inputs also participate the generation of SV Pul cell response properties. In contrast to SV neurons, the response properties of S and V neurons are more specific in that they distinguish between retinal image motion generated by saccades and motion in the external world. It seems unreasonable that such response properties result from pretectal input, because pretectal neurons do not show this differentiation in their responses between externally and internally generated image motion. More likely sources for the generation of such elaborate response properties are cortical areas that also provide visual input to the Pul. For example, neurons that respond to visual stimuli but not to saccades and vice versa have been described in area PMLS (Yin and Greenwood 1992a,b) from which another direct projection to the LP-P arises (Updyke 1981). 217 Functional considerations In cat, no direct evidence that would support any welldefined Pul function is available. Although Pul neurons showed significant differences in their responses to the stimuli used in our study, all three neuronal populations identified could be involved in the modulation of visual information flow when saccadic eye movements are executed. The different Pul cell response properties may reflect the fact that neuronal activity in different Pul target structures has to be modulated specifically according to their own functional roles in the visual pathway. Thus, S neurons could provide a strong signal that indicates the appearance of a new visual surround as a result of saccadic eye movements to cortical areas, or they could generate saccadic suppression in cortical areas if their activity is fed into appropriate inhibitory circuits. However, because we must assume that these cells do not receive significant visual input, we can only speculate on the origin of saccade-related input to S neurons. As their responses did not show any obvious selectivity for saccade parameters, providing information about the occurrence of a saccadic eye movement may be more important than coding any saccade parameter. The activation of V neurons, which are able to discriminate between either externally or internally generated retinal image motion, could lead to facilitation of visual responses after saccades in visual cortical areas. SV neurons, which do not distinguish between external image motion and saccades, could more globally induce arousal in visual cortical areas after changes of visual surround following both self-induced eye movements or external motion. In monkey, a function in the guidance of visual attention has been proposed for the Pul (Robinson et al. 1991). Because of evident analogies in response properties between neurons in the Pul of cats and monkeys, the cat Pul may also integrate visuomotor information in an attentional context. Acknowledgements We wish to thank K.P. 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